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THE 


VELIGER 


A Quarterly published by 

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC. 
Berkeley, California 

R. Stohler, Founding Editor 


Volume 36 


January 4, 1993 to October 1, 1993 


TABLE OF CONTENTS 


Number 1 (January 4, 1993) 


Systematic position of three European heterobranch gastropods 
ANDERS WAREN, SERGE GOFAS, AND CHRISTOFFER SCHAND- 
1h De oe air anerengetr inn aracnorseor tad inég tio eb ak Baa 6-056 6-0 o-ono-o 1 
Three new Halgerda species (Doridoidea: Nudibranchia: Opis- 
thobranchia) from Guam 
C..H CARLSON AND! P.. J. HOFF 5 52. Shae ee he 16 
New species and records of Lepetodrilus (Vetigastropoda: Lepe- 
todrilidae) from hydrothermal vents 
JAMES HE MCICEANS 35 ase ieee ee 27 
A defensive value of the thickened periostracum in the Mytiloidea 
E. M. HARPER AND P. W. SKELTON ................ 36 
Morphological and allozyme variation in Littorina sitkana and 
related Littorina species from the northeastern Pacific 
ELIZABETH GRACE BOULDING, JOHN BUCKLAND-NICKS, AND 
KATHERINE LYN VAN ALSTYNE ................-.. 43 
A new Ashmunella (Gastropoda: Pulmonata: Polygyridae) from 
Sonora, Mexico 
RICHARD ULE: IREEDER) fags aiieie en neces ee ea aes 69 
First Oligocene records of Calyptogena (Bivalvia: Vesicomyidae) 
JAMES L. GOEDERT AND RICHARD L. SQUIRES ........ 72 
A new Muricopsis from the Gulf of California, Mexico 
BARBARA W. MYERS, CAROLE M. HERTZ, AND ANTHONY 
DvATTUIO wc cis heen ee te one ere eho pee oes eae 78 


First report of the ovulid gastropod Sulcocypraea mathewsoniu 
(Gabb, 1869) from the Eocene of Washington and Oregon 
and an additional report from California 

RICHARD L. SQUIRES AND LINDSEY T. GROVES ....... 81 

New records for ranellid gastropods in the western Atlantic (Ra- 
nellidae: Cymatiinae) 

BEDRTY JEAN PIECH, (55-4) oo ae ee 88 

Predation by Latzaxis oldroydi (Gastropoda: Coralliophilidae) on 
Corynactis californica (Anthozoa: Corallimorphidae) 

Mary K. WICKSTEN AND ROBERT T. WRIGHT 

Invasion of the south Texas coast by the edible brown mussel 
Perna perna (Linnaeus, 1758) 

Davip W. HICKs AND JOHN W. TUNNELL, JR. ....... 92 

Brooding of larvae in Cardita aviculina Lamarck, 1819 (Bivalvia: 
Carditidae) 

JAAS SCHNEIDER. 3030 hen eee 94 

In situ spawning behavior of an Alaskan population of pinto 
abalone, Haliotis kamtschatkana Jonas, 1845 

MICHAEL S. STEKOLL AND THOMAS C. SHIRLEY 


Number 2 (April 1, 1993) 


Population structure of two common species of ascoglossan (= 
sacoglossan) opisthobranchs on the central coast of Oregon, 
USA 

CYNTHIA D. TROWBRIDGE ................-.....-.. 99 

Fine structure of the three cell types found in the digestive gland 
of Elysia viridis (Opisthobranchia: Sacoglossa) 

REGINA GRIEBEL 107 

Behavioral interactions among nudibranchs inhabiting colonies 
of the hydroid Obelia geniculata 

WALTER J. LAMBERT 115 

Redescription and taxonomic reappraisal of the tropical Indo- 
Pacific nudibranch Siraius nucleola (Pease, 1860) (Antho- 
branchia: Doridoidea: Dorididae) 

GILIANNE D. BRODIE AND RICHARD C. WILLAN 124 

Polygyrid land snails, Vespericola (Gastropoda: Pulmonata), 1. 
Species and populations formerly referred to Vespericola 
columbianus (Lea) in California 

BARRY ROTH AND WALTER B. MILLER 134 

Slugs of Portugal. III. Revision of the genus Geomalacus Allman, 
1843 (Gastropoda: Pulmonata: Arionidae) 

T. RODRIGUEZ, P. ONDINA, A. OUTEIRO, AND J. CASTIL- 
LEJO 145 


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The taxonomic status of Buccinanops d’Orbigny, 1841 (Gastrop- 
oda: Nassariidae) 
GuIDO PAsTORINO 160 
Formation of organic sheets in the inner shell layer of Gelozna 
(Bivalvia: Corbiculidae): an adaptive response to shell dis- 
solution 
SHINJI IsajI 166 
A new species of Cypraea from Samoa in the C. cribraria complex 
C. M. BURGESS 174 
How does Strombina reproduce? Evidence from two Venezuelan 
species (Prosobranchia: Columbellidae) 
ROBERTO CIPRIANI AND PABLO E. PENCHASZADEH .... 178 
A review of the genus Kaiparathina Laws, 1941 (Mollusca: Gas- 
tropoda: Trochoidea) 
BRUCE A. MARSHALL 185 
Prey attack by the Patagonian octopus Octopus tehuelchus d’Or- 
bigny: an odd pattern 
OsCAR IRIBARNE, MIRIAM FERNANDEZ, MARINA DIAZ, AND 
MARINA CLEMENTE 199 
Examples of damage repair in the shell of the cephalopod genus 
Argonauta 
KENT D. TREGO 


Number 3 (July 1, 1993) 


Energetic implications of variation in pedal mucus production 
by Patella vulgata Linnaeus, 1758 
Mark S. DAVIES 203 
Application of a two-dimensional electrophoresis method to the 
systematic study of Notaspidea (Mollusca: Opisthobran- 
chia) 
RYOKO TSUBOKAWA AND JUN-ICHI MIYAZAKI 209 
Karyotype and nucleolus organizer regions in Ostrea puelchana 
(Bivalvia: Ostreidae) 
ANA INSUA AND CATHERINE THIRIOT-QUIEVREUX .... 215 
Variability in growth and age structure among populations of 
ribbed mussels, Geukensia demissa (Dillwyn) (Bivalvia: My- 
tilidae), in Jamaica Bay, New York (Gateway NRA) 
DaviD R. FRANZ AND JOHN T. TANACREDI 220 
Maturation processes in female Loligo bleekeri Keferstein (Mol- 
lusca: Cephalopoda) 
GYEONG HUN BAEG, YASUNORI SAKURAI, AND KENJI SHIMA- 
ZAKI 228 
A comparison of larval development, growth, and shell mor- 
phology in three Caribbean Strombus species 
MeEGAN Davis, CYNTHIA A. BOLTON, AND ALLAN W. 
STONER 236 
Studies on the reproduction and gonadal parasites of Fissurella 
pulchra (Gastropoda: Prosobranchia) 
MarTA BRETOS AND RICARDO H. CHIHUAILAF 245 
Genital dimorphism in the land snail Chondrina avenacea: fre- 


quency of aphally in natural populations and morph-specific 
allocation to reproductive organs 
BRUNO BAUR AND XIAOFENG CHEN 252 
A new species of Otostoma (Gastropoda: Neritidae) from near 
the Cretaceous/Tertiary boundary at Dip Creek, Lake Na- 
cimiento, California 
RICHARD L. SQUIRES AND LOUELLA R. SAUL 259 
The nautilid Eucymatoceras (Mollusca: Cephalopoda) in the Lower 
Cretaceous of northern California 
PETER U. RoppDA, MICHAEL A. MURPHY, AND CLARENCE 
SCHUCHMAN 265 
Earliest record of the anomiid bivalve Pododesmus: a new species 
from the lower Eocene of western Washington 
RICHARD L. SQUIRES 270 
Relict shells of Subantarctic Mollusca from the Orange shelf, 
Benguela region, off southwestern Africa 
JOHN PETHER 276 
The gastropods in the streams and rivers of four islands (Guad- 
alcanal, Makira, Malaita, and New Georgia) in the Solo- 
mon Islands 
ALISON HAYNES 285 
Ampullariid phylogeny—book review and cladistic re-analysis 


RUDIGER@BIEGERS. Aoe eras dee re te ae ees 291 
Questionable species in the cephalopod genus Argonauta 
SENT HD)! REGO! ee ter cn a eis Meee cose ensee reo das ce wouaw. 298 


Number 4 (October 1, 1993) 


Local and regional abundance patterns of the ascoglossan (= 
sacoglossan) opisthobranch Alderia modesta (Lovén, 1844) 
in the northeastern Pacific 

CYNTHIA D. TROWBRIDGE 303 

The influence of olfactory and tactile stimuli on the feeding 
behavior of Melibe leonina (Gould, 1852) (Opisthobranchia: 
Dendronotacea) 

WINSOR H. WATSON III AND CHARLES M. CHESTER .. 311 

Ecological, morphological, and genetic differences between the 
sympatric bivalves Donax variabilis Say, 1822, and Donax 
parvula Philippi, 1849 

WALTER G. NELSON, ERIK BONSDORFF, AND LAURA ADAMKE- 
WICZ 317 

New reports of the large gastropod Campanile from the Paleocene 

and Eocene of the Pacific coast of North America 
RICHARD L. SQUIRES 323 

Larval morphology of the scallop Argopecten purpuratus as re- 

vealed by scanning electron microscopy 
GILDA BELLOLIO, KARIN LOHRMANN, AND ENRIQUE DU- 
PRE 332 

A review of Pitar (Hyphantosoma) Dall, 1902 (Veneridae: Pi- 

tarinae) and a description of Pitar (H.) festoui sp. nov. 


MONS” 1SIVMAN IGUNSNS Yoconeabsoceeces sean uouage® 343 
Additions to Pacific Slope Turonian Gastropoda 
L. R. SAUL AND W. P. POPENOE .................. 351 


Atlanta californiensis, a new species of atlantid heteropod (Mol- 
lusca: Gastropoda) from the California Current 
ROGER R. SEAPY AND GOTTHARD RICHTER 


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The gastropod Terebra santana Loel & Corey, 1932, from the 
lower Miocene Vaqueros Formation, southern California, 
belongs in the cerithiid genus Clavocerithium s.s. 

RICHARD L. SQUIRES 399 

The validity of Chaetoderma montereyense Heath along with Ch. 
argenteum Heath (Mollusca: Caudofoveata) 

LUITFRIED V. SALVINI- PLAWEN 405 

An empirical evaluation of various techniques for anesthetization 
and tissue fixation of freshwater Unionoida (Mollusca: Bi- 
valvia), with a brief history of experimentation in molluscan 
anesthetization 

C. CLIFTON CONEY 413 

Effects of restricted food intake on hemolymph glucose concen- 
tration and digestive gland-gonad lipid level in the schis- 
tosome vector Biomphalaria glabrata (Say) (Gastropoda: 
Planorbidae) 


S. N. THOMPSON AND V. MEJIA-SCALES ............ 425 
Aggressive behavior of the whelk Morula musiva. 
INIAOV-AUAIB Ee iyeyaee ee ratio enti nye soubctiay sen cists Wing ttcccay alle 428 


Band color pattern on the venter of a mature shell of Nautilus 
pompilius Linnaeus, 1758 
KENT D. TREGO 431 
Range extension for the land snail Eremarionta rowelli hutsoni 
(G. H. Clapp, 1907) 
JAMES E. HOFFMAN 


AUTHOR INDEX 


JABES SING 52 cet SSA PRR nee CSE REA 428 
ADAMKEWIGZ.01s. 52-2. 2 sn hee ee See ae eee 317 
BAEGS (Git FI e ionic succack HOPS eee 228 
BAUR NIB Sint ka net air gn ae Cir er SS 252 
BELEOLION Gis seo eee ee ee ee en eee ee 332 
IBERTSCHS Fle ic. 50 eaten tse tae dace ea re cen (301) 
IBIELER, (Ro 5 Sete een ote Fee ee ee een RoE Tea 291 
BOE TON CVA 8 noo Neen eect ea ae anh cece ae 236 
BONSDORER SEs, © ces stares Ee ee ee 317 
IBOWEDING 52h)! Gileros ee Farce ae Raa aioe eae 43 
BRETOSs Mi 9 elec ee ence ea ROR ona te ae nena as 245 
BRODIE: Gr De po coc yen ice yay aee ee eRe wo eae 124 
BUCKLEAND=NICKS yp: 5 ee ied eee race rea eieway se wae 43 
BURGESS) 3 Gi Mila a) 9 spa eee eee a ie ee a ee 174 
CARESONS (Gia. ih cease see aed es pee 16 
GASTILER OS ees eal ee eee Ee ee 145 
GENS a aie Rei a th cerca rah ot ome ire mie ena 252 
CHESTER, Gi Mey. ate ear ene eee ae oe ree 311 
(Cie tisiOPNIUND Teel gaa onodeeadnaaeunontesedaeaas 245 
GIPRIANT ARS: a7 8 eps os See ee er ee ee 178 
GEEMENTES Missile eh. alee ie be ee lee ns comto aan 199 
GONEY Ci © ator HN trai a cue tee gte ANTS EU eRe 413 
DZATTILIO MAC aye ke ee Pecan are on en er nt a ene 78 
IBAVITES CIN AS a7 eRe pe ta etch mae ete ar eae eae eee eee Re 203 
TAVIS MIR cee ar 2 ar Souk eo a ree ee can ae eee a a ae 236 
Te) LAZAR irayrss 5 pecs cec eS eT es ee ot 199 
J UPRIE OE St eee rhe ce ac aces eee ROO ed ee eee 332 
IPERNAND EZ gta en are cee ay eae ei rn eee ae 199 
EVRUAIN ZAR) eR ape ah oracle te Sy Sr ay OY go ee PRR Pe 220 
GOEDERTA palit yori me cana ee cca re eee ore i2. 
GOPAS TS 5h esacathe ene cli gey eis Babee Sy qt tty PER Re Miss Sein 1 
GRIEBE DR Re cin sonata ath tee go cacy os ter haa Ep Sea 107 
GROVES SRE: Ae oo NP ie a gin ele er ee ecg ete 81 
TAR PER = BiB ee ay one gen tat inert Steet oe ee ae Re ae tre oe 36 
EVAR TESS ICUS Ste ee eats Aare See Se pai ee a AE a 343 
IEVAYINES A cane ice fetete as rat ans aap Tie ey are ae re per ee 285 
FER Z1 Giese ee cecoe eae cen et eR ar ay ad a ee efea e 78 
ERICK MANS I @ SS 2s ces oes CE ee ease (98) 
FLICKS RW hee oe can eea tt cp aii aoa eae ee iE 92 
1s (0) 31 ed ea eee eenee erate oman eviccesic tas rac tate eeu ers tro e 16 
TIOREMAN, oJ: vice. uetite canter ta: olsee die Meena ee 431 
TINSWA SHAS Aor orien a soe Nt eras ot as yn eet fe eee 215 
TRIBARNE; | @) ev cc) pct wus ac eesacie o1 o eEOR 199 
SAUTTERS x ch Beh See el Sg EA SE es BR 166 
IGAMBER TW). Jie <, fteh ok pod epee Carrs etree heen 115 
TEOHRMANN SK) Po go a ee gene ret ee ae oes a eee 332 
IMIARSHATL 1B Arta) Acide eee Le eee eee 185 


MICIZEAN (JH nes I a ee as ee) ee ee 27 
MIE JIA-SCALES Vio hoc caee eee 425 
MUEEERS OW) Be ieee cen 2 shel des cache tack ee 134 
MUYAZAKIN Jel) os oy oe eee ee ee 209 
MURPHY, M2 As 202525 Ge eS Oe ee 265 
MIVERSS Bi OWao6 hoc oe eae 78 
INELSON! (Wi Ge 20 ies eee ee 317 
QNDINA; Be io es 8 sc a oo re ee 145 
QUTEIRO} Avis pies od ose Scare 145 
PASTORINO, (Gin sco oi ooh ne Be eee 160 
PENCHASZADEH, Ps eo eee 178 
PETHER, (Jiitihy 2208) gt ase Oa See eee 276 
PIECH,, B: Jin 5 saw an care bs ee eee 88 
POPENOE, Wii Bits 2d canes eee 351 
REEDER, Re Tes... oshac yi ek oe eee 69 
RICHTER; Gis. 8) bw eee 389 
RoOpDA; Pino ens ana ok See eee 265 
RODRIGUEZ, Rs iis 632... eee 145 
ROTH) Be): 2 2s. bP ee ee ee ee 134 
SAKURAI} Yeo. nk oS a eee 228 
SALVINI-PLAWEN, I) Valu css. So eee 405 
SAUL ORS 230 ere ese ase eee 259, 351 
SCHANDER, ©. .= 286.0 020 an oe eee 1 
SCHNEIDER, J.:Av. 0 200. cae cout el ee ee eee 94 
SCHUGHMAN, Coe 53 Mal. ee ieee 265 
SEAPY,“R. Rios bn te dine eg eee 389 
SHIMAZAKIS Ke) Sloss acs ¢ See 228 
SHIREEY;, TF) 2.5 woklce. sos Soa ee eee 95 
SKELTON, Ps Won. ecco doen: hol eRe 36 
SS OUWIRIES Ss Rese lis erate naa a 72, 81, 259, 270, 323, 399 
STEKO MGcS) . ej Os ones 2 oe Ae ee 95 
STONER AGW). cecce os Sones ae el eee 236 
TANAGREDI,. J); Tes cad ooh oe Ue oe 220 
THIRIOT-QUIEVREUX, ©. 7° 2 5.. 5) eee 215 
"THOMPSON; SiON. 4.09 ali ciao eae 425 
IEREGCOR KG ee oh oat sao tee ae 200, 298, 430 
TROWBRIDGE, © De eee oe 99, 303 
TSUBOKAWA, R: 0. 30. 2a Se eee eee 209 
RUNNELL,. JR: J We ot so E es ee eee 92 
VAN ALSTYNE, Ke 0 es a 43 
VOIGHT) {Ji Road otc Oh nea oe eee (433) 
VOKES) (EeHic.ce ai ok ie so eee (302) 
WAREN; ‘Al ois 2 ee ee Ee eee 1 
WATSON; TID, We Hi 22s) gee a eee 311 
WIGKSTEN; MLK ose ino ee 92 
WILLAN; RaG@. exe. sae se ee 2 8 as ee ee 124 
WRIGHT, Ree eee ss cpt Cnn on 92 


Page numbers for book reviews are indicated by parentheses. 


lv 


LL 


O| 


i els 


“VELI 


A Quarterly published by 

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC. 
Berkeley, California 

R. Stohler, Founding Editor 


ISSN 0042-3211 


Volume 36 January 4, 1993 Number 1 


CONTENTS 


Systematic position of three European heterobranch gastropods 
ANDERS WAREN, SERGE GOFAS, AND CHRISTOFFER SCHANDER .......... 1 


Three new Halgerda species (Doridoidea: Nudibranchia: Opisthobranchia) from 
Guam 
Crees CARTSON VAN Ddhy soe ORE ge ao pags dhe idee cielo ile eas cys Gagiyedda evs 16 


New species and records of Lepetodrilus (Vetigastropoda: Lepetodrilidae) from 


hydrothermal vents 
J/AMGIS) Le Le IAI ISIN, isc ec a a TF ae a ele ee Dall 


A defensive value of the thickened periostracum in the Mytiloidea 
ep ViEg EVARPERYVAND Pu SKELTON Giri s eS m oye bon Ao rs he Go Se 36 


Morphological and allozyme variation in Littorina sitkana and related Littorina 
species from the northeastern Pacific 
ELIZABETH GRACE BOULDING, JOHN BUCKLAND-NICKS, AND KATHERINE LYN 
NZAN@ANIES ION EM ep any ROME Ree ey ek Cyan NOE seas ben ole e 43 


A new Ashmunella (Gastropoda: Pulmonata: Polygyridae) from Sonora, Mexico 
REL ETANRITD) ora ERE ESD) ER step yes eles layla Sh velar gates Aa Ne ie ey ere cecal cae) dh eS 69 


First Oligocene records of Calyptogena (Bivalvia: Vesicomyidae) 
AMES EG OEDERDANDERICHARDY IL: ;SQUIRES..4.2)) 46 cu- 44525025 4G 54. 72 


A new Muncopsis from the Gulf of California, Mexico 
BARBARA W. MYERS, CAROLE M. HERTZ, AND ANTHONY D’ATTILIO ..... 78 


CONTENTS — Continued 


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The Veliger 36(1):1-15 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Systematic Position of ‘Three European 


Heterobranch Gastropods 


ANDERS WAREN 


Swedish Museum of Natural History, Box 50007, S-10405 Stockholm, Sweden 


SERGE GOFAS 


Laboratoire de Malacologie, Museum National d’Histoire Naturelle, 
55, Rue de Buffon, F-75005 Paris, France 


CHRISTOFFER SCHANDER 


Department of Zoology, University of Goteborg, Medicinaregatan 18, 
S-41390 Goteborg, Sweden 


Abstract. The external morphology of the soft parts, the shell, and the radula are described for the 
two Mediterranean gastropod species Oxystele depressa Granata (formerly in the Skeneidae) and Skenea 
pellucida Monterosato (formerly in the Skeneopsidae). Oxystele depressa is transferred to Tomura Pilsbry 
& McGinty, 1946 (Cornirostridae). Skenea pellucida is made the type of Xenoskenea Warén & Gofas, 
gen. nov., and classified in the family Hyalogryinidae, a heterobranch family with rhipidoglossate radula. 
Noerrevangia fragilis Warén & Schander, gen. et sp. nov. (Cornirostridae) is described from shallow 


water around the Faeroe Islands. 


INTRODUCTION 


Small, globular or low spired, “‘skeneimorph” and “‘vitri- 
nellid-like” gastropods have for many years presented great 
problems for authors trying to classify them (Mediterra- 
nean species reviewed by GHISOTTI, 1984). The species 
have frequently been transferred between genera like Ske- 
nea, Daronia, Cyclostrema, Skeneopsis, Tubiola, Vitrinella, 
Teinostoma, and others. WAREN (1992) attempted to sta- 
bilize the classification of some of the European species, 
mainly those belonging to the ““Archaeogastropoda.” This 
paper deals with three additional species belonging to the 
Heterobranchia. 

Examination of living specimens of Oxystele depressa 
Granata and Skenea pellucida Monterosato showed that 
these species cannot belong to the families or genera where 
they previously were classified (Skeneidae and Skeneop- 
sidae; SABELLI e¢ a/., 1990), but have to be classified in two 
recently established families, Cornirostridae Ponder, 1990b, 
and Hyalogyrinidae Warén & Bouchet, 1992. 


Noerrevangia fragilis gen. et sp. nov. (described herein) 
was found by Schander during field work at the Faeroe 
Islands. From the external morphology of the soft parts 
and from radular morphology this species fits well in the 
Cornirostridae. 

The Cornirostridae and Hyalogyrinidae, in which these 
species are included, are not very well known to most 
malacologists, and the Heterobranchia, where they are 
classified, has been considerably enlarged during the last 
three years by the addition of a number of new families 
(listed herein, see ‘““Systematics”). We therefore give a short 
supplement to the discussion by PONDER (1991) on this 


group. 


MATERIALS anp METHODS 


This paper is partly based on observations made on live 
specimens of Oxystele depressa and Skenea pellucida during 
field work. Color drawings were prepared and notes were 
based on weakly anesthetized specimens observed under a 


Page 2 


stereomicroscope with a drawing tube. The observations 
are supplemented by the examination of shells from various 
collections. Noerrevangia fragilis was obtained in sedi- 
ment residues fixed in formalin during field work in the 
Faeroe Islands, and it was not possible to examine the 
specimen alive. The soft parts were therefore extracted, 
stained with carm-alum, and examined under a stereo- 
microscope. Afterwards they were critical point dried and 
examined with scanning microscopy. Subsequently the soft 
parts were rehydrated and the radula extracted by dis- 
solving the tissues in KOH. 

The material we have had access to is listed under each 
species, with the location of the material: BMNH—Nat- 
ural History Museum, London; MNHN—Muséum Na- 
tional d’Histoire Naturelle, Paris; SMNH—Swedish Mu- 
seum of Natural History, Stockholm; USNM—United 
States National Museum of Natural History, Washington, 
D.C. 


SYSTEMATICS 
Subclass Heterobranchia 


PONDER (1991) discussed the following superfamilies and 
families as being of importance for the understanding of 
early heterobranch phylogeny: 


Valvatoidea: Valvatidae, Orbitestellidae, Cornirostridae 
(see PONDER, 1990a, b, 1991; HEALY, 1990) 

Architectonicoidea: Architectonicidae, Mathilididae 

Pyramidelloidea: Pyramidellidae, Amathinidae 

Omalogyroidea: Omalogyridae 

Rissoelloidea: Rissoellidae 

Glacidorboidea: Glacidorbidae (PONDER, 1986). 


Four families have afterwards been added to the early 
heterobranchs: 


Provalvatidae Bandel, 1991 (Valvatoidea; fossil, Juras- 
sic) 

Hyalogyrinidae Waren & Bouchet, 1992 (superfamily 
uncertain) 

Tjaernoeidae Waren, 1991 (superfamily uncertain) 

Xylodisculidae Warén, 1992 (superfamily uncertain). 


New heterobranch families based on the genera Ebala 
Gray, 1847 (Pyramidelloidea) and Cima Chaster, 1897 
(unknown superfamily) are in the process of being de- 
scribed (Warén, unpublished). 

PONDER & WAREN (1988) and PONDER (1991) favored 
an opinion that the Heterobranchia and Caenogastropoda 
were independently derived from different ‘‘archaeogas- 
tropod” groups and that the archiotaenioglossates repre- 
sent an early offshoot of the branch leading to the caenogas- 
tropods. The recognition of the family Hyalogyrinidae 
(WAREN & BOUCHET, 1992), with many heterobranch 
characters (Haszprunar, in preparation) and a rhipido- 
glossate radula strongly supports Ponder’s view, rather 
than the scenario proposed by HASZPRUNAR (1988), who 
considered the heterobranchs and caenogastropods to be 


The Veliger, Vol. 36, No. 1 


derived from a common ancestor, above the archaeogas- 
tropod level. 

The detailed relations between the families listed above 
and the “subclasses” Pulmonata and Opisthobranchia are 
still incompletely known. 

At present the most important task for increasing the 
knowledge about the lower heterobranchs is to extract, 
from the muddle of small “‘archaeo-” and caenogastropods, 
the right candidates for further exploration of the “missing 
links” between, on one side the ‘“‘archaeo-” and caenogas- 
tropods, and on the other side between the “archaeogas- 
tropods” and the heterobranchs. 


Family CORNIROSTRIDAE Ponder, 1990 


Remarks: The family Cornirostridae was erected by 
PONDER (1990b) for the genera Cornirostra and Tomura, 
which are characterized by the following synapomorphies 
(in addition to a number of anatomical characters, which 
have not been examined in the species discussed herein 
and therefore cannot be evaluated): 


—a bifurcate snout 

—an anteriorly bifurcate foot 

—a posteriorly bifurcate foot 

—a single right pallial tentacle 

—a bipectinate, basally attached ctenidium 

—a hermaphroditic reproductive system with cephalic pe- 
nis 

—production of gelatinous egg masses 

—a central radular tooth with highly developed lateral 
supports 

—two or three partly overlapping lateral teeth. 


The species of Cornirostridae are astonishingly similar 
to species of Vitrinellidae in their shell characters. Some 
species, for example Tomura depressa, can be recognized 
as belonging to the Heterobranchia by their heterostrophic 
larval shell, but an examination of the radula is usually 
needed to confirm the familial position. 

Ponder interpreted the radula of Cornirostra to be tae- 
nioglossate, but we consider PONDER’s (1990b:534, 543) 
“accessory plate” to be a third lateral tooth (PONDER, 
1990b:figs. 4A, E). 

In the same way it can be seen from PONDER’s (1990b) 
fig. 3A of Tomura bicaudata Pilsbry & McGinty, that each 
row consists of nine teeth. The two lateral teeth are stuck 
together, but in fig. 3D, the outer lateral tooth has been 
bent towards the marginal tooth (to the right). In our 
Figure 9 this is more obvious, since the serrated lateral 
margin of the inner lateral tooth can be distinguished. 

We therefore assume that Cornirostra and Tomura bi- 
caudata have nine teeth per transverse row. Ponder (per- 
sonal communication) has agreed with this interpretation. 

It can also be seen from PONDER’s (1990b) fig. 4D and 
E of Cornirostra that it is only the most lateral tooth which 
folds laterally when the radula is “opened.” This is also 
our experience from Tomura depressa (Figures 7, 10). (In 


A. Waren et al., 1993 


T. bicaudata the two outer teeth fold laterally.) In a tae- 
nioglossate radula this unfolding takes place between the 
second and third tooth, and the two marginal teeth will 
be folded laterally. Consequently the radular formula of 
Cornirostra should be 1:3:1-3-1 and that of Tomura (bi- 
caudata) 2:2-1-2-2 or (depressa) 1:2:1-2:1. 

In the Orbitestellidae the transverse rows of teeth consist 
of five teeth (PONDER, 1990a). We can therefore not agree 
that these radulae are taenioglossate. This does not, how- 
ever, disturb the relations between the Cornirostridae and 
the Valvatidae, because the presence of a rhipidoglossate 
radula in Xenoskenea, Hyalogyra, and Hyalogyrina sug- 
gests the presence of such a radula in the early hetero- 
branchs and that the taenioglossate condition of the valvatid 
radula is not homologous to that of the Caenogastropoda, 
although the radulae have the same number of teeth. 

Noerrevangia fragilis also has the formula 2:2:1-2-2. 
Such a radula, as well as that of Cornirostra and Tomura, 
may have evolved from a rhipidoglossate-like radula sim- 
ilar to that of the Hyalogyrinidae. 


Tomura Pilsbry & McGinty, 1946 


Tomura PItsBRY & McGInTy, 1946:15. Type species, by 
monotypy Virtrinella (Tomura) bicaudata Pilsbry & 
McGinty, 1946 (Florida). 


Remarks: The crawling animal and the shell of the type 
species were figured by PILsspry & McGINTYy (1945:pl. 2, 
fig. 9) and described in some detail by PONDER (1990b), 
based on topotypic material. 

Tomura depressa differs from the type species in having 
one tooth less in the marginal field and by having a shell 
with an umbilicus. This will probably turn out to be of 
generic value, but since at present these two species are 
more similar to each other than to any other known species, 
we prefer not to introduce additional generic names before 
we can see a need for it. 


Tomura depressa (Granata, 1877) 
(Figures 1-11) 


Oxystele depressa GRANATA, 1877a:146; GRANATA, 1877b:9. 
Tharsiella tinostomoides FEKIH & GOUGEROT, 1977:224. 


Type material: Oxystele depressa, not known; Tharsiella 
tinostomoides, holotype and 1 paratype from the type lo- 
cality, 5 paratypes from Tunisia, Porto Farina, in MNHN. 


Type localities: Oxystele depressa, Sicily, Strait of Mes- 
sina, 65 m; Tharsiella tinostomoides, Gulf of Tunis, Khéred- 
dinne. 


Material examined: Tunisia: Golfe de Gabés: NW of 
Mer de Bou Grara, diving, 10-15 m, 150 shells (MNHN); 
Canal d’Ajim, diving 10-32 m, 10 shells, 2 specimens 
(SMNH); Djerba, SE of El Kantara, 4-5 m, 3 shells 
(MNHN)); Sfax, 3 shells, Jeg. Gougerot (MNHN); Gulf 
of Tunis, Porto Farina, 20 shells, Jeg. Gougerot (MNHN). 


Page 3 


FRANCE: Corsica, Baie de Calvi, algal washing, 10-40 
m, 2 shells (SMNH); Marseille, off Mejean, 37 m, 2 shells 
(MNHN). 

ITALy: Livorno, off Capraia, 180 m, coll. F. Giusti, 1 
shell; Sicily, Catania, Acitrezza, shell gravel, 36 m, 3 shells 
(SMNH); Sicily, Bay of Brucoli, 17 m, 1 specimen 
(MNHN). 

SpaIN: Malaga, dredged in 20-40 m, 2 shells (MNHN). 


Distribution: Throughout the Mediterranean and Rabat 
(Atlantic Morocco), usually in 10-50 m (OLIVERIO, 1982, 
1985, 1988; our material). Shells commonly found, live- 
taken specimens rare. 


Redescription: The shell (Figures 1, 2) is very small, 
Natica-like, with an umbilical callus, transparent and rath- 
er solid. The larval shell (Figure 3) is hyperstrophic, di- 
ameter 150-175 wm. Protoconch I is only partly visible, 
and is mainly sculptured by a system of branching and 
anastomosing small ridges, except close to the demarcation 
to protoconch II. Protoconch II is almost smooth with only 
a few incremental lines and spirally arranged granulae, 
and consists of about 0.7 whorl. The teleoconch consists 
of about 2.0 whorls, usually almost perfectly smooth, sep- 
arated by a very indistinct and shallow suture. Occasional 
specimens differ in having the initial part of the teleoconch 
equipped with a few spiral ridges (Figure 4), but this 
character varies in strength. The aperture is prosocline, 
almost tangential with the inner lip spread out to form a 
solid parietal and umbilical callus. 

Dimensions: Maximum diameter 1.6 mm. 

Operculum (Figure 117): It is thin and transparent, mul- 
tispiral with short growth zone and central nucleus. 

Radula (Figures 7-10): Formula 1-2-1-2-1. The radula 
is rather short and broad with about 20 transverse rows. 
The marginal tooth is broad and flat, roughly rectancular, 
with the distal end slightly obliquely truncated and den- 
ticulate. The outer, distal corner is slightly drawn out and 
cusplike, and the outer side of the tooth is finely denticulate 
almost to its base. The outer lateral tooth is short, rounded 
with the inner corner somewhat drawn out. This tooth is 
denticulate along its outer and apical sides. The inner 
lateral tooth is broad, apically evenly rounded and finely 
denticulate all around. The central tooth has a pair of 
lateral, wing-shaped supports and a central, distinct sup- 
porting ridge. The triangular cutting edge is serrated with 
about 9-11 denticles on each side of a central cusp. When 
tilted backwards, the distinctive anterior furrow becomes 
more obvious. 

Soft parts (Figures 5, 6): The animal is almost colorless 
except for the pale brownish digestive gland and milky 
white cells in the anterior pedal gland. A small, bright 
yellow pigmented mantle organ is visible, dorsally and 
immediately behind the gill, through the shell. The foot is 
large, broad, thin, anteriorly expanded with drawn-out 
corners and is shallowly bifurcate; the sides are otherwise 
parallel; posteriorly it has a deep U-shaped notch, giving 
the posterior end a bifid appearance. The propodium is 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 1 to 4 


Figures 1-4. Tomura depressa, Canal d’Ajim, between Djerba and mainland, Tunisia. Figure 1. Apical view, 1.25 
mm. Figure 2. Front view, 1.36 mm. Figure 3. Larval shell, diameter 171 wm. The arrow indicates the demarcation 
of protoconch I and II. Figure 4. Unusually strongly sculptured specimen, diameter of larval shell 152 um. 


not demarcated from the mesopodium; the metapodium 
(opercular lobe) forms a thin fold between the operculum 
and the mesopodium, hanging free between the two “tails.” 
The head is small and slender, with long, cylindrical ten- 
tacles; the eyes are very small and deeply buried in the 
tentacle bases. A small, elongate, slightly tapering penis is 
attached laterally just to the right of the right cephalic 
tentacle. The snout is long and cylindrical, distally deeply 
bifurcate; a pair of jaws can be seen through the trans- 
parent central part of the snout. A minute pallial tentacle 
is present at the right corner of the pallial margin. The 
ctenidium is triangular, bipectinate, and attached basally. 


Remarks: OLIVERIO (1982, 1985, 1988) reviewed the 
Mediterranean species Tharsiella romettensis (Granata) and 


T. depressa (Granata), their nomenclatorial history, and 
their distribution, but kept them both in Tharsiella, clas- 
sified in the Skeneidae. For comments on Tharsiella, which 
is a junior synonym of Cirsonella Angas, 1877 (provision- 
ally in Skeneidae) and 7. romettensis, see WAREN (1992). 

Our description of the soft parts is based on two spec- 
imens observed alive. One, examined in the Golfe de Gabes, 
Tunisia, was taken on a sandy bottom in Canal d’Ajim, 
between Jerba and the mainland. The second specimen 
was taken on a sandy bottom off Brucoli in eastern Sicily, 
at 17 m depth. The rarity of live specimens is probably 
because the precise habitat is still unknown. 

The external morphology of the head-foot of 7omura 
depressa agrees well with that of the type species of Tomura 
(cf. Figures 5, 6 with PONDER 1990b:fig. 2), but the shell 


A. Waren et al., 1993 


Page 5 


9 


Explanation of Figures 5 and 6 


Figures 5, 6. Tomura depressa, crawling animal. Sicily, off Brucoli, 17 m depth. Penis, jaws, eyes, and ctenidium 


visible through transparent tissues. 


differs from 7. bicaudata in lacking the umbilicus, which 
in 7. depressa is filled out by a callus. PONDER (1990b) 
did not, however, find a pigmented mantle organ in 7. 
bicaudata and the pallial tentacle is shorter in 7. depressa. 

The shell of TZomura depressa has the appearance of a 
miniaturized Natica with an umbilical callus, but exami- 
nation of the larva shell shows that the initial whorl is 
very small, tilted, and depressed. Furthermore, the di- 
ameter of the protoconch is less than 0.2 mm, whereas the 
larval shell of European species of Naticidae with an um- 
bilical callus has a diameter of about 1 mm or larger— 
1.e., comparable to the size of an adult 7. depressa. 


Noerrevangia Waren & Schander, gen. nov. 


Type species: Noerrevangia fragilis Warén & Schander, 
sp. nov. 


Diagnosis: Small, Vitrinella-like cornirostrids with a pau- 
cispiral protoconch of half a whorl, and radular formula 
2-2-1-2-2. Penis exceptionally large, equipped with open 
seminal gutter (Figure 19). 

Description: See specific description of Noerrevangia fra- 
gilis. 

Etymology: Named after Professor Arne Norrevang, di- 


rector of the Kaldbak Marine Laboratory at the Faeroe 
Islands. 


Remarks: The systematic position of Noerrevangia is not 
obvious from the shell. The anteriorly and posteriorly di- 
vided foot, the bifurcate snout, and the radular morphology 
do, however, indicate relations with the Cornirostridae. 
Additional similarities, although less diagnostic, are the 
right pallial tentacle, the presence of a cephalic penis, the 
bipectinate ctenidium, and the shape of the shell. 

The shell and the head-foot of Noerrevangia closely 
resemble those of Cornirostra, but the spire of Noerrevan- 
gia is much more depressed and the penis of Noerrevangia 
has an open seminal gutter (internal in Cornirostra). We 
have therefore introduced a new genus. 

The radulae of Tomura and Cornirostra differ from that 
of Noerrevangia in the number of the marginal teeth (two 
in Noerrevangia, one or two in Tomura, and one in Cor- 
nirostra), the number of lateral teeth (two in Noerrevan- 
gia, three in Cornirostra, two in Tomura), and the shape 
of the inner lateral tooth, which has two main cusps in 
Noerrevangia. (The two cusps of the first lateral tooth of 
N. fragilis may, however, be the result of fusion of two 
teeth.) The central tooth of the three genera shows great 
similarity in the development of the winglike lateral pro- 
cesses. 

The protoconch of Noerrevangia is not similar to that 
of the other cornirostrids, but since there is no trace of a 
protoconch II, the development can be assumed to be leci- 
thotrophic. In connection with a change from plankto- 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 7 to 13 


Figures 7-13. Radulae and opercula. Figures 7-11. Tomura depressa, Canal d’Ajim, between Djerba and the 
mainland, Tunisia. Arrows indicate indistinct borders between teeth; numbers indicate the sequence of the teeth, 
with the central tooth as number one. Figure 7. Vertical view. Scale line 10 um. Figure 8. Another view of marginal 
teeth. Scale line 10 wm. Figure 9. Posterior view of central and lateral teeth. Scale line 5 wm. Figure 10. Vertical 
view of another specimen. Scale line 5 um. Figure 11. Operculum, diameter 0.88 mm. Figures 12, 13. Xenoskenea 
pellucida, operculum, Sicily, diameters 0.46 mm and 0.91 mm. 


A. Waren et al., 1993 


Page 7 


Explanation of Figures 14 to 17 


Figures 14-17. Noerrevangia fragilis gen. et sp. nov., holotype. Figures 14-16. Shell, diameter 1.7 mm. Figure 


17. Larval shell diameter 270 um. 


trophic development to lecithotrophic, great changes in the 
shape of the protoconch are common and we consider this 
difference of minor importance. 

Although seemingly a minor detail, the fact that the 
penis is lying parallel to the cephalic tentacle may signify 
an important character. Almost all caenogastropods keep 
the penis folded backwards, so it lies along the right corner 
of the pallial cavity. The position may, however, also be 
a preservation artifact. 


Noerrevangia fragilis 
Waren & Schander, sp. nov. 
(Figures 14-25) 


Type material: Holotype (now badly broken) SMNH 
4423. 


Type locality: The Faeroe Islands, off Thorshavn, 
62°04.5'N, 06°42.8’W, 43 m, clay bottom. 


Material examined: Known only from the holotype. 


Distribution: Known only from the type locality at the 
Faeroe Islands, in 43 m depth. 


Etymology: Fragilis (Latin), meaning “fragile.” 


Description: The shell (Figures 14-16) is small, trans- 
parent, vitrinellid-like with a depressed spire, and is very 
fragile. The larval shell (Figure 17) consists of slightly 
more than half a whorl with a diameter of 270 um. It is 
low and depressed in shape and there are traces of a finely 
granular sculpture on the initial part, but this area is 
slightly corroded in the unique specimen. The teleoconch 
consists of 2.0 whorls of a rounded cross section, slightly 


Page 8 


Explanation of Figures 18 to 20 


The Veliger, Vol. 36, No. 1 


Bas 


Figures 18-20. Noerrevangia fragilis gen. et sp. nov., holotype, critical point dried. Figure 18. Contracted head- 
foot, anterior view. Scale line 100 wm. Figure 19. Penis, ventral view, showing the seminal furrow. Scale line 50 
um. Figure 20. Snout and cephalic tentacle, surface structure. Scale line 25 wm. Key: CT, cephalic tentacle; P, 


penis; S, snout. 


indented by the preceding whorl. The sculpture consists 
of rather indistinct and slightly flexuous incremental lines. 
The suture is distinct but not depressed since the outer lip 
makes a distinct adapical deviation from its circular shape, 
evening out the transition to the preceding whorl. The 
aperture is distinctly prosocline and the outer lip slightly 
sinuated just below the suture. The umbilicus is broad and 
deep and penetrates the shell to the protoconch. 

Dimensions: Diameter 1.7 mm. 

Operculum: Round, stiff, colorless, multispiral and 
smooth, with central nucleus. 

Radula (Figures 21-25): Formula 2-2:1-2+2. Central 
tooth with a sturdy, pointed, and serrated cutting edge and 
winglike basal supporting ridges. The first lateral tooth is 
very broad and has two cutting plates, one rounded and 
more central and one more pointed at the midpoint of the 
tooth. Lateral to this cutting plate the tooth has a winglike 
lateral protrusion. The second lateral tooth is very broad 
and has a rounded, serrated cutting plate occupying the 
inner one-third of the apical margin. The two marginal 


teeth are oarlike, long, slender, and serrated along the 
apical one-third, where they have a thin web along the 
edge. 

Soft parts (Figures 18-20): The foot is anteriorly deeply 
divided and the corners are drawn out laterally. The pro- 
podium is narrow and inconspicuous. Posteriorly the foot 
does not taper regularly to a point, but probably is deeply 
notched, as in Jomura (but should could not be ascertained 
because of the contraction of the preserved animal). No 
epipodial ridges or tentacles were noticed. The snout is 
long, slender, and bifurcate to half its length. The cephalic 
tentacles are only sparsely ciliated, are slightly longer than 
the snout, and lack sensory papillae. Pigmented eyes are 
lacking. The large penis, attached just behind the right 
cephalic tentacle, is twice as broad and slightly longer than 
the tentacle. Its anterior, ventral edge has a deep seminal 
groove (Figure 19) that lies along the cephalic tentacle. 
The pallial edge is smooth and simple. Its right corner has 
a richly ciliated pallial tentacle of half the length of the 
cephalic tentacles. The ctenidium, which is large and bi- 


Explanation of Figures 21 to 25 


Figures 21-25. Noerrevangia fragilis gen. et sp. nov., radula of the holotype. Numbers indicate the sequence of 
the teeth, with the central tooth as number 1. Arrows indicate borders between teeth. Figure 21. Oblique view of 
central and lateral teeth. A marginal tooth (4) is concealing the outer part of the outer lateral tooth. Scale line 10 
um. Figure 22. Oblique view of central and lateral teeth. The point of the more anterior central tooth (1) is 
concealed by a marginal tooth. Scale line 5 wm. Figure 23. Oblique view of central and lateral teeth. Lateral “wing” 
of central tooth broken. Scale line 5 wm. Figure 24. Oblique view of lateral teeth. Slightly different angle of Figure 
21. Seale line 5 wm. Figure 25. Complete radula, length 215 um. 


A. Waren et al., 1993 Page 


Page 10 


pectinate, occupies two-thirds of the width of the pallial 
cavity in the holotype. The digestive gland is richly spotted 
with brown granules. 


Remarks: The shell of this new species is featureless and 
it would presently be impossible to classify it from con- 
chological characters only. Among European genera it re- 
sembles Skeneopsis (Skeneopsidae), but species of that ge- 
nus have a reddish or brownish, more solid shell with a 
deeper suture, and a protoconch of slightly more than one 
whorl sculptured with spiral lines and granules. We il- 
lustrate the shell, protoconch, and radula of the type species 
for comparison (Figures 37-41). 

The more archaeogastropod-like genus Akritogyra Wa- 
rén, 1992 (systematic position uncertain, provisionally in 
Skeneidae), resembles Cornirostra and Noerrevangia, but 
the shell has a slightly taller spire and the species have a 
rhipidoglossate radula with the formula 4-6-2-1-2-4-6 
(WAREN, 1992). The soft parts of Akrztogyra are still poorly 
known. 


Family HYALOGRYINIDAE Waren & Bouchet, 1992 


Two genera (Hyalogyra and Hyalogyrina, both described 
by MARSHALL, 1988) and four species are so far known 
to belong to this family (MARSHALL, 1988; WAREN & 
BOUCHET, 1992). These species live on pieces of sunken 
driftwood or at hydrothermal vents, in fairly deep water, 
1000-2000 m. 

The species are characterized by: 


—a rhipidoglossate radula 

—a bipectinate ctenidium 

—heavily ciliated areas on the tentacles 

—an absence of epipodial tentacles 

—the protoconch, if multispiral, is hyperstrophic. 


The tentacular arrangement is still uncertain. Anatom- 
ical work on Hyalogyrina and the new genus described 
below is being carried out by G. Haszprunar. 


Xenoskenea Waren & Gofas, gen. nov. 


Type species: Skenea pellucida Monterosato, 1874, Medi- 
terranean. 


Diagnosis: Heterobranchs with Vitrinella-like, small, de- 
pressed, perfectly transparent, and almost smooth shell. 
Protoconch indistinctly hyperstrophic. Teleoconch with 2- 
3 evenly rounded whorls. Foot large, anteriorly expanded 
and shallowly bifurcate, posteriorly abruptly drawn out 
into a narrow, tentacle-like point. Snout large and cylin- 
drical, with small tentacle distally on each side. Right 
corner of pallial cavity modified to a large pad, covering 
part of the preceding whorl. Gill bipectinate. Radula rhip- 
idoglossate with formula n-3-1-3-n. 


Description: See the description of Xenoskenea pellucida. 


Etymology: Xenos (Greek), meaning “strange,” and Ske- 
nea (Skeneidae), an archaeogastropod genus with a shell 
imilar to the type species. 


The Veliger, Vol. 36, No. 1 


Remarks: Hyalogyra differs from Xenoskenea in having 
a more depressed shell with more shallow suture. Hyalo- 
gyra also lacks the tentaclelike appendages on the snout 
and has three tentacles on the head. 

Hyalogyrina also differs from Xenoskenea in lacking the 
distal appendages of the snout, by having short appendages 
between the cephalic tentacles or a long appendage lat- 
erally to the right cephalic tentacle, and by having a radula 
with a single row of lateral! teeth on each side of the center. 

The shell of Xenoskenea is very similar to that of Cor- 
nirostra, but has a flexous profile of the outer lip, instead 
of being straight and radial. Furthermore, Cornirostra pel- 
lucida has a long, slender right pallial tentacle, whereas 
Xenoskenea has a pad covering a part of the early part of 
the body-whorl, and Cornirostra has a bifurcate snout, 
whereas Xenoskenea has a cylindrical snout with two 
tentaclelike appendages. Also the radulae are widely dif- 
ferent: Xenoskenea has a rhipidoglossate radula, whereas 
that of Cornirostra has the formula 1-3-1-3-1. 

There are some assumed archaeogastropods which are 
very similar to Xenoskenea, for example Akritogyra Wa- 
ren, 1992 (provisionally in Skeneidae), but their larval 
shell has a proportionally larger initial part, which is not 
sunken in the center (see WAREN, 1992:fig. 15A-F). This 
difference may, however, be due to lecithotrophic devel- 
opment in the species of Akritogyra. The external mor- 
phology of their soft parts and their anatomy is still largely 
unknown. 

The radula and shell of a new species probably be- 
longing to Xenoskenea were described from off Luanda 
(Angola) by Rusio et al. (in press). The species was clas- 
sified in Hyalogyra Marshall, but differs from Xenoskenea 
pellucida only in the shape of the central tooth. We there- 
fore believe that this species belongs to Xenoskenea. The 
specimens were found on a dead fish from the bottom, and 
were assumed to be feeding on the carrion. 

Xenoskenea pellucida was previously tentatively clas- 
sified in Skeneopsis Iredale, 1915 (Skeneopsidae), a genus 
of littorinoidean affinity (PONDER, 1988). We illustrate 
the shell, protoconch, and radula of the type species for 
comparison (Figures 37-41). 

Relying on shell morphology, PONDER (1990b:537) sug- 
gested that Skenea pellucida may belong to the Corniros- 
tridae. This is not supported by the radular morphology. 

The second European species of Skeneopsis, S. sultano- 
rum Gofas, 1982, remains in Skeneopsis, based on obser- 
vations of living animals (Gofas, unpublished data). 


Xenoskenea pellucida (Monterosato, 1874) 
(Figures 12, 13, 26-36) 


Skenea pellucida ARADAS & BENOIT, 1874:159 (nom. nud.). 

Skenea pellucida MONTEROSATO, 1874:263. 

Skenea helicina Jeffreys MS, MONTEROSATO, 1874:263 (in- 
troduced in synonymy). 

Skenea pellucidoides NORDSIECK, 1982:46. 

Skeneopsis pellucida: GOFAS, 1982:232, fig. 8. 

Skeneopsis ? pellucida: PONDER, 1990b:537. 


A. Waren et al., 1993 


Page 11 


Explanation of Figures 26 to 30 


Figures 26-30. Xenoskenea pellucida, Tunisia, Bou Grara Sea. Figure 26. Basal view, diameter 1.56 mm. Figure 
27. Apical view of adult specimen, diameter 1.59 mm. Figure 28. Apical view of young specimen, diameter 1.03 
mm. Figure 29. Front view, adult specimen, diameter 1.64 mm. Figure 30. Larval shell, diameter 245 wm. 


Type materials: Skenea pellucida, lectotype (GOFAS, 1982) 
and 5 paralectotypes in MNHN. Skenea pellucidoides, ho- 
lotype and 1 paratype, Baleares, Ibiza, 50 m and 2 para- 
types, Tunisia, Sfax, in Senckenbergisches Museum und 
Forschungsinstitut, Frankfurt a.M. 


Type localities: Skenea pellucida, Sicily, Palermo; S. pel- 
lucidoides, Baleares, Ibiza, 50 m. 


Material examined: PORTUGAL, Algarve: Sagres harbor, 
9-15 m, rocks with ooze, 4 shells (MNHN); Sagres, Ponta 
dos Caminhos, 23-33 m, 1 shell (MNHN); Sagres, Bay 
de Baleeira, 12-17 m, 1 shell (MNHN); Chenal d’Olhao, 
3-7 m, in mud covered with Zostera, about 20 specimens 
(SMNB). 

(Morocco) CEUTA: El Pineo, 35°52.6'N, 05°19.7'W, 9- 
10 m, 1 shell (MNHN). 


Page 12 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 31 and 32 


Figures 31, 32. Radula of Xenoskenea pellucida, Brucoli, Sicily. Figure 31. Detail of lateral and central teeth. Scale 


line 5 um. Figure 32. Overview, scale line 10 um. 


Morocco: Near Oued er Rmel, 35°53.3’N, 05°30.2’W, 
13 shells (MNHN). 

ALGERIA: Algiers, coll. Jeffreys, 1 shell (USNM 145049). 

Tunisia: Djerba, Borj Jillij, 0-8 m, among Poszdonia, 
2 shells (MNHN); Canal d’Ajim, 10-32 m, 5 shells 
(SMNH); Bou Grara Sea, littoral, 13 shells (MNHN). 

ITALY: Gulf of Naples, coll. Jeffreys, 2 shells (USNM 
185037); Sicily, no further details, 7 shells (SMNH); Sici- 


ly, Trapani, from Monterosato, 4 shells (BMNH); Sicily, 
Magnisi, Palermo, coll. Jeffreys, 4 shells (USNM 185036); 
Sicily, S of Catania, Brucoli, Posidonia beds, 2 specimens 
(MNHN); Sicily, no further details, 6 + 10 shells, coll. 
Jeffreys (USNM 185035 and 202425). 

FRANCE: Corsica, Baie de Calvi, algal washing, 10-40 
m, | shell (SMNH). 


A. Warén et al., 1993 


Page 13 


Explanation of Figures 33 to 35 


Figures 33-35. Xenoskenea pellucida, Portugal, Algarve, Ria de Olhao, Zostera bed, 3 m. Diameter of shell 1.7 


Imm. 


GREECE: Patrai lagunar area, 2 shells, leg. Nofroni 
(MNHN),. 


Distribution: Western and central Mediterranean, to 
southern Portugal, ca. 0-25 m, on muddy algal bottoms. 


Redescription: The shell (Figures 26-29) is Valvata-like, 
small, fragile, completely transparent, smooth except for 
some growth lines. The larval shell (Figure 30) consists 
of about 0.75 whorl of rapidly increasing diameter, and 
its maximum diameter is 250 um. Its initial part is com- 
paratively small and indistinctly hyperstrophic. The te- 
leoconch consists of up to 2.3 whorls of almost circular 
cross section, sculptured by sharp, basally flexuous incre- 
mental lines. The suture is deep. The area in contact with 
the preceding whorl occupies 20-30° of the cross section 
of the whorl and makes a slight dent in the circular shape 
of the peristome. The umbilicus is deep and wide, and 
permits examination of the protoconch. 

Dimensions: Maximum diameter 2.0 mm. 

Radula (Figures 31, 32): The radula is rhipidoglossate 
with the formula n-3-1-3-n. The central tooth has di- 
verging lateral supports and a slender, triangular cutting 
surface. The first lateral tooth is similar to the central but 
has a single lateral support and its inner side fits into a 
groove between the supporting ridge and “back” of the 
central tooth. The second lateral tooth is similar to the 


first one. The third lateral tooth is much broader and the 
outer part of its cutting edge is serrated. The marginals 
are at least 10 in number, tall and slender, distally oblique- 
ly truncated, and deeply serrated. 

Operculum (Figures 12, 13): Thin, colorless, and mul- 
tispiral with central nucleus. 

Soft parts (Figures 33-36): The foot is large and thin, 
anteriorly expanded and shallowly bifurcate. The sides are 
parallel, except the anterior and posterior extremities. Pos- 


Figure 36 


Xenoskenea pellucida, young specimen, Sicily, Brucoli, Posidonia 
bed, 3 m depth. Diameter of shell 1.1 mm. 


Page 14 


The Veliger, Vol. 36, No. 1 


“4 


Explanation of Figures 37 to 41 


Figures 37-41. Skeneopsis planorbis. Figures 37-39. Shells. Ceuta, Anse Sarchal, intertidal. Diameters 1.3, 1.2, and 
1.2 mm. Figure 40. Larval shell. Corsica, Calvi, Punta Revellata, intertidal. Diameter 290 um. Figure 41. Radula. 


Norway, Finmark, intertidal. Scale line 10 um. 


teriorly it is abruptly drawn out into a narrow tentacle. 
The propodium is not externally differentiated. Just be- 
hind the corners of the foot, the propodium contains an 
opaque, yellowish mass of cells close to each side, and 
centrally there is a group of whitish, superficial spots con- 
sisting of glandular cells. The metapodium forms a bilobed 
skin fold between the operculum and the foot. The snout 
is large and cylindrical, apically truncated with a centrally 
situated mouth and a short, cylindrical tentacle on each 
side. The buccal mass and radula are visible through the 
transparent snout. The tentacles are long and slender, 
slightly tapering and lack sensory papillae. The black eyes 
are embedded in the center of the bases of the tentacles. 
The penis is small, situated just behind and slightly lateral 
to the right eye. The pallial margin is simple, dark gray 


to black, and reflected over the edge of the peristome, 
especially at the left corner of the aperture. The right 
corner of the pallial cavity is modified to a large gray, 
black, or dark brown pad, covering a part of the preceding 
whorl. The edge of the mantle and the apertural pads are 
superficially dark gray; the upper part of the snout and 
the tentacles are only slightly tinged with the same color. 
The gill is bipectinate with more than 20 pairs of leaflets. 
It is attached basally, and protrudes from the pallial cavity 
when the animal is crawling. In live specimens the food- 
string could be observed in the upper part of the intestine, 
rotating clockwise. 


Remarks: Xenoskenea pellucida appears to be a rare spe- 
cies, judging from the literature, but this is probably a 


A. Warén et al., 1993 


collecting bias because it lives on shallow, muddy seagrass- 
and algal bottoms, which are only rarely examined for this 
small size range of gastropods. 

The shell of Xenoskenea pellucida is just as featureless 
as the soft parts are characteristic, but there are no species 
known in shallow Mediterranean waters with which it is 
likely to be confused. 

CARROZZA (1976:fig. 7) used the name Skenea pellucida 
for an unusually smooth specimen of Skeneopsis planorbis 
(Fabricius, 1780). 

Xylodiscula boucheti Warén, 1992 (Xylodisculidae, Het- 
erobranchia) is superficially similar but has a flatter spire 
and broader umbilicus, and lives in deeper water. It has 
a very different radula with no central tooth. 


ACKNOWLEDGMENTS 


We thank W. F. Ponder and G. Haszprunar for critically 
reading and commenting on the paper. P. Bouchet and B. 
Metivier arranged the workshops, where we found the two 
Mediterranean species and assisted in the field work. C.S. 
wants to thank the Nordic Council of Marine Biology and 
Prof. A. Norrevang, the Faeroes, who made his work in 
the Faroes possible. C. Hammar (SMNH) prepared the 
photographic prints. 

A.W. wants to thank ‘““Magnus Bergwalls Stiftelse” for 
economic support for this and other work on the mollusks 
of northern Europe. 


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marine valvatoidean (Gastropoda: Heterobranchia). Journal 
of Molluscan Studies 56:533-555. 

PONDER, W. F. 1991. Marine valvatoidean gastropods—im- 
plications for early heterobranch phylogeny. Journal of Mol- 
luscan Studies 57:21-32. 

PONDER, W. F. & A. WAREN. 1988. Classification of the Cae- 
nogastropoda and Heterostropha—a list of the family group 
names and higher taxa. Malacological Review, Supplement 
4:288-326. 

Rusio, F., E. ROLAN & F. FERNANDES. In press. Nueva especie 
de Hyalogyra (Archaeogastropoda: Skeneidae) procedente de 
la costa occidental Africana. Bollettino Malacologico. 

SABELLI, B., R. GIANNUZZI-SAVELLI & D. BEDULLI. 1990. An- 
notated check-list of Mediterranean marine mollusks. 1. Edi- 
zione Libreria Naturalistica Bolognese. 348 pp. 

WarREN, A. 1991. New and little known Mollusca from Iceland 
and Scandinavia. Sarsia 76:53-124. 

WaREN, A. 1992. New and little known “skeneimorph”’ gas- 
tropods from the Mediterranean Sea and the adjacent At- 
lantic Ocean. Bollettino Malacologico 27:149-247. 

WarEN, A. & P. BOUCHET. 1992. New records, species, genera, 
and a new family of gastropods from hydrothermal vents 
and hydrocarbon seeps. Zoologica Scripta 21. 


The Veliger 36(1):16-26 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Three new Halgerda species 
(Doridoidea: Nudibranchia: Opisthobranchia) 


from Guam 


C. H. CARLSON anp P. J. Horr! 


The Marine Laboratory, University of Guam, Mangilao, Guam 96923 


Abstract. 


Halgerda tessellata (Bergh, 1880) is reported from Guam and Pohnpei within the Micro- 


nesian area and three new species of Halgerda are described. Two are compared with H. aurantiomaculata 
(Allan, 1932) and H. terramtuentis Bertsch & Johnson, 1982, both previously described white tuberculate 
forms. The third is compared with the type species of the genus, 7. formosa Bergh, 1880. 


INTRODUCTION 


The genus Halgerda Bergh, 1880a (= Dictyodoris Bergh, 
1880b) contains dorids with a somewhat smooth, stiff ge- 
latinous texture with a reticulate pattern of dorsal ridges 
which may or may not have tubercules at their points of 
juncture. Recent discussion of the genus can be found in 
RUDMAN (1978) and WILLAN & BRODIE (1989). Since 
1969, 10 species of Halgerda have been collected on Guam, 
including one dredged from 120 m. Six of the species are 
represented by only one or two specimens in the authors’ 
collection. Of the remaining four, one has been previously 
described, BERGH (1880b), and three are described in this 


paper. 
SPECIES DESCRIPTIONS 
Halgerda tessellata (Bergh, 1880) 
(Figures 1-3) 


Dictyodoris tessellata BERGH, 1880b:75-78, pl. C, figs. 11- 
12; pl. F, figs. 22-23; Exvior, 1905:229-230; Burn, 
1975-5115: 

Halgerda tessellata (Bergh): RUDMAN, 1978:65-67, figs. 4C— 
D, 6; WILLAN & COLEMAN, 1984:38-39, 52. 


Distribution: Halgerda tessellata was originally described 
from Palau (7—-8°N, 134°E) in the Western Caroline Is- 
lands. Halgerda tessellata has also been reported from Aus- 
tralia (BURN, 1975), Madagascar (ELIOT, 1905), and Ke- 
nya (RUDMAN, 1978). Since 1969, 87 specimens of H. 


Present address: P.O. Box 8019, Merizo, Guam 96916. 


tessellata have been found on Guam (13°N, 145°E) and an 
additional two on Pohnpei (7°N, 158°E) in the Federated 
States of Micronesia. The average depth has been 8 m, 
with the deepest found at 15 m. Two have been found on 
the reef flat. The largest measured specimen was 33 mm. 
The records from Guam and Pohnpei extend the range 
both north and east in the Micronesian area. The only 
other Halgerda recorded with such a wide Indo-Pacific 
distribution is H. wasinensis Eliot, 1904. It has been re- 
ported from the Tanzanian-Kenyan area of east Africa 
(ELIOT, 1904; RUDMAN, 1978) and the Marshall Islands 
(JOHNSON & BOUCHER, 1983). 


Color: In most specimens, the body color, as seen from 
the foot, underside of mantle and mantle margin, varies 
from yellow to yellow-orange (Figures 1, 2). Except for a 
broad marginal band, most of the dorsum is covered by 
dark brown pigment. The brown pigment is less dense 
over the ridges giving them a mustard yellow to orange- 
brown appearance. Scattered opaque white dots occur in 
the depressions between the ridges. These dots become 
denser toward the outer edge of the brown. Scattered dark 
brown spots are on the sides of the foot and underside of 
the mantle. There is also a broad dark brown line on the 
mid-dorsal part of the tail. The rhinophores are translucent 
white with a dark brown posterior streak. The lamellae 
are dark brown. The branchia are white with some of the 
upper surface of the rachis dark brown. The ridge coloring 
is not as red as that shown on the color plate in WILLAN 
& COLEMAN (1984:39, fig. 118). One of the specimens 
from Pohnpei (Figure 3) had a translucent white rather 
than yellow body and less of the brown pigment. 


C. H. Carlson & P. J. Hoff, 1993 


Explanation of Figures 1 to 3 


Figures 1-3. Halgerda tessellata. Figure 1. 14-mm specimen, Guam, Bile Bay, 14 m depth, 13 June 1971. Figure 
2. 23-mm specimen, Guam, Bile Bay, 2 July 1984. Figure 3. 33-mm specimen, Pohnpei, 8 m depth, 17 October 


1987. 


Halgerda guahan Carlson & Hoff, sp. nov. 
(Figures 4-9) 


Halgerda graphica Basedow & Hedley: CARLSON & Horr, 
1973:6, fig. 5 (misidentification). 


Specimens: Since 1969, 59 specimens of Halgerda guahan 
have been found on Guam. The average depth was 8 m, 
the maximum 15 m. One specimen was found on the reef 
flat. The average length of those measured was 43 mm, 
the longest 64 mm. 


Type material: Holotype (64 mm), Bishop Museum, Ho- 
nolulu, BPBM 209916, reef flat, Cetti Bay, Guam, 18 
June 1988, Carlson and Hoff. Paratype (47 mm), Bishop 
Museum, Honolulu, BPBM 209917, 11 m depth, Bile 
Bay, Guam, 16 March 1991, Carlson and Hoff. Material 
dissected: 1 specimen, 32 mm, 15 m depth, Agat, Guam, 
Carlson and Hoff, 21 March 1969; 1 specimen 35 mm, 
Bile Bay, Guam, Carlson and Hoff, 17 December 1978; 
1 specimen 53 mm, 12 m depth, Bile Bay, Guam, Carlson 
and Hoff, 29 October 1982; 1 specimen, 45 mm, 9 m depth, 
Bile Bay, Guam, Carlson and Hoff, 16 March 1991. Rad- 


ulae of the 35-mm and 45-mm specimens were used for 
scanning electron micrography. 


External morphology: The living animals (Figures 4, 5) 
are ovate. A 38-mm specimen had a maximum width of 
21 mm, others were 46 X 25 mm and 53 X 26 mm. The 
body has a firm gelatinous texture, as is found in all other 
members of the genus. It is convex, sloping gradually from 
the thin mantle margin to the mid-dorsum. The broad, 
flaring mantle is slightly irregular and usually lies along 
the substrate when the animal is crawling. The dorsum 
has a series of low ridges and depressions with no tubercles. 
A central ridge extends from just in front of the rhinophores 
almost to the branchia. Two polygonal ridged areas are 
on either side of this medial ridge and an incomplete po- 
lygonal area contains the rhinophores. Other ridges extend 
transversely from the polygons toward the mantle margin. 
Shallow depressions occur within each polygon and be- 
tween the transverse ridges. The ridges have 16 major 
points of convergence; four along the midline and six on 
either side. The foot (Figure 6) is a little over one-third 
of the width of the animal (8 mm for a 21 mm wide 


Page 18 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 4 and 5 


Figures 4, 5. Halgerda guahan sp. nov. Figure 4. 32-mm specimen, Guam, Agat Boat Channel, 15 m depth, 21 
March 1969. Figure 5. 48-mm specimen, Guam, Anae Island, March 1991. 


specimen) and it ends in a rounded tail that is sometimes 
visible when the animal is crawling. The anterior of the 
foot has a transverse groove with the upper lamina split 
in the middle. The oral tentacles are digitiform. 

The base of the rhinophores is short and stocky; the 
club is thin and angled posteriorly. The branchia has four 
gills; the posterior two being divided about one-third of 
the way up from the base. The branchial and rhinophoral 
sheaths are low and simple. 

The body is translucent white, almost transparent on 
the mantle margin. The pinkish brown to purplish brown 
color of the viscera is visible through the dorsal surface. 


Figure 6 


Halgerda guahan sp. nov., ventral view, 48-mm living specimen. 


The mantle margin is edged by a thin, opaque white line. 
All ridges are edged in yellow. Single, irregular, curved 
yellow lines appear within the depressions. No lines extend 
to the edge of the mantle. The rhinophores are translucent 
white with brown spots on the base and lamellae. On some 
specimens the posterior of the rhinophoral base has a broad 
brown line, which continues as brown streaks on the pos- 
terior parts of the lamella. The rhinophoral sheath is edged 
in yellow. The branchia are translucent with scattered 
white extending up the rachis and on the tips. Sparse 
brown spots also appear on the branchia. The branchial 
sheath is white with yellow lines that extend up from the 
body. The underside of the body, foot, and oral tentacles 
are translucent white. Some specimens have a small brown 
dot between the upper and lower lamina at the anterior 
of the foot. 

Specimens possessing color variations have been found. 
These variations appear to be the result of damage to the 
dorsal surface, which causes the yellow lines on the ridges 
to become broken and irregular. 

Specimens preserved in alcohol have retained the brown 
pigment but not the yellow. In one specimen, which had 
been fixed in 5% formalin and stored in alcohol for two 
years, the ridges became pink. It can also be seen on the 
preserved specimens that the yellow lines within the dorsal 
depressions actually covered low ridges. 


Internal morphology: The sac of tissue enclosing the 
viscera, which appears dark in slides of living specimens, 
is transparent with brown flecks. With the sac opened 
dorsally, the large oval stomach, the intestine, the digestive 
gland mass, and the prostate-covered bursa copulatrix are 
visible. With the blood gland and nerve ring removed, the 
white oral tube can be seen curving to join the heavy 
muscular buccal bulb. With the stomach moved slightly 
to the right, the broad curved radular sac can be seen 
extending from the ventral posterior of the buccal bulb. 
The esophagus exits from the buccal bulb, makes a dorsal 


Gwe Carlsoniceseys ielott, 1993 


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Page 19 


Paa85 15KY 


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Explanation of Figures 7 and 8 


Figures 7, 8. Halgerda guahan sp. nov. Figure 7. Scanning electron micrograph of middle lateral teeth, 45-mm 
specimen. Figure 8. Scanning electron micrograph of outermost lateral teeth, 45-mm specimen. Figure 8A. Camera 
lucida drawing of outermost lateral teeth, 32-mm specimen. Scale = 10 um. 


loop and enters the stomach ventrally. The intestine exits 
from the anterior of the stomach and curves around the 
right side of the digestive gland and continues posteriorly 
to the anus. From the dorsal view, the top of the brownish 
prostate-enclosed bursa copulatrix and the albumen/mu- 
cous (female) gland complex can be seen to the right and 
anterior to the stomach. The aorta passes from the blood 
gland, crosses and is attached to the top of the prostate- 
covered bursa copulatrix. It continues under the intestine 
and extends posteriorly to the heart at the anterior base 
of the branchia. 

The radular formulae for 32-mm and 45-mm adult 
specimens were 50 X 49-0-49 and 46 x 45-47-0-45-47 
respectively. All teeth except the outer three laterals are 
simply hamate with a flange on the inner edge. In the 32- 


mm specimen, the inner 20 teeth were small and gradually 
increased in size toward the center of the half row (Figure 
7). There were 26 large teeth of approximately the same 
size and then three small outer laterals. The innermost 
lateral was smaller than the outermost. The scanning elec- 
tron micrograph shows the outermost laterals to be flat- 
tened plates with the outer two having slightly irregular 
apices (Figure 8). When viewed with a compound micro- 
scope the innermost of these three teeth appeared irregular 
at the apex, the penultimate tooth appeared slightly den- 
ticulate, and the outermost was very thin and apically 
denticulate (Figure 8A). 

Within the reproductive system (Figure 9), the her- 
maphroditic duct connects to the ampulla posterior to the 
genital mass. The broad ampulla appears as a convoluted, 


Page 20 


fhe See 


Figure 9 
Halgerda guahan sp. nov., Reproductive system: al-mu, albumen- 
mucous gland; am, ampulla; bc, bursa copulatrix; p, penis; pr, 


prostate; rs, receptaculum seminis; ud, uterine duct; vd, vas de- 
ferens; vg, vaginal duct. 


somewhat flattened tube at the posterior of the prostate 
and the albumen/mucous gland complex. It narrows and 
enters the genital mass at the gland complex, where it joins 
the prostate gland. The whitish prostate gland ensheathes 
and folds down under the bursa copulatrix. The actual 
point of entry of the duct from the ampulla was not ob- 
served. A narrow duct arises from the same area, and 
divides into two ducts; one, the uterine duct, extends for- 


The Veliger, Vol. 36, No. 1 


Figure 12 


Halgerda malesso sp. nov., ventral view, 65-mm living specimen. 


ward, where it enters the bursa copulatrix; the other leads 
to the receptaculum seminis, which is embedded in the 
prostate gland between the bursa copulatrix and the female 
gland complex. The long thin tube to the ovoid recepta- 
culum seminis forms a loop along the gland complex and 
joins the receptaculum seminis posteriorly. Adjacent to the 
entry of the uterine duct into the bursa copulatrix is the 
vaginal duct, leading to the vagina which is enclosed in a 
muscular sheath with the smaller penis. The vagina has 
a series of longitudinal folds. The long sinuous vas deferens 


Explanation of Figures 10 and 11 


Figures 10, 11. Halgerda malesso sp. nov. Figure 10. 64-mm specimen, Guam, Anae Island, 8 m depth, 27 April 
1969. Figure 11. 48-mm specimen, Guam, Toguon Bay, 18 m depth, 11 April 1969. 


C. H. Carlson & P. J. Hoff, 1993 


13 
200800 


14.A 


Page 21 


CHB8he 15KY xX 


I-—_4 


Explanation of Figures 13 and 14 


Figures 13, 14. Halgerda malesso sp. nov. Figure 13. Scanning electron micrograph of innermost lateral teeth, 55- 
mm specimen. Figure 14. Scanning electron micrograph of outermost lateral teeth, 55-mm specimen. Figure 14A. 
Camera lucida drawing of outermost lateral teeth, 64-mm specimen. Scale = 10 um. 


extends from the small penis to the prostate where it en- 
sheaths the bursa copulatrix. A broad extention from the 
female gland mass leads to the genital opening, where it 
terminates in the oviduct. The vagina, penis, and oviduct 
share a common opening through the body wall. 


Discussion: Halgerda guahan differs from previously de- 
scribed white and orange species of Halgerda in that it 
lacks tubercles, has an uncolored mantle and foot margin, 
and has a comparatively simple pattern of lines on the 
dorsum. Internally, the narrow vagina and penial sac en- 
closed in a muscular sheath differ from the large vagina 
and large penial sac of both H. aurantiomaculata (Allan, 
1932) and H. terramtuentis Bertsch & Johnson, 1982. 
The specific name guahan is the Chamorro (z.e., the 
indigenous people of Guam) name for the island of Guam. 


Halgerda malesso Carlson & Hoff, sp. nov. 
(Figures 10-15) 


Specimens: Since 1969, 117 specimens of Halgerda ma- 
lesso have been found on Guam and an additional six on 
the island of Sarigan (17°N, 146°E) in the Northern Mar- 
iana Islands. The average depth was 9 m, with the deepest 
recorded, 18 m. The average length of those measured was 
48 mm, the longest was 65 mm. 


Type material: Holotype (49 mm), Bishop Museum, Ho- 
nolulu, BPBM 209914, 14 m depth, Bile Bay, Guam, 24 
April 1991, Carlson and Hoff. Paratype (65 mm), Bishop 
Museum, Honolulu, BPBM 209915, 15 m depth, Bile 
Bay, Guam, 20 April 1991, Carlson and Hoff. 


Page 22 


1mm 


Figure 15 


Halgerda malesso sp. nov. Reproductive system: al, albumen gland; 
am, ampulla; be, bursa copulatrix; bw, body wall; go, genital 
opening; mu, mucous gland; po, penial opening; pr, prostate; ps, 
penial sheath; rs, receptaculum seminis; ud, uterine duct; v, ves- 
tibule; vd, vas deferens; vg, vagina; vo, vaginal opening. 


Material dissected: 1 specimen, 64 mm, 8 m depth, 
Anae Island, Guam, Carlson and Hoff, 27 April 1969; 1 
specimen 55 mm, 7 m depth, Bile Bay, Guam, Carlson 
and Hoff, 13 July 1988; 1 specimen, 60 mm, 14 m depth, 
Bile Bay, Guam, 24 April 1991. Radulae of the 60-mm 
and 55-mm specimens were used for scanning electron 
micrography. 

External morphology: The living animals (Figures 10, 
11) are ovate with a broad, thin, slightly undulating mantle 
edge. A 55-mm specimen was approximately 30 mm wide 
at the broadest point. As is true of other species of Halgerda, 
the body texture is gelatinous, smooth, and firm. The dor- 
sum has three distinct, irregular, longitudinal ridges with 
elevated tubercles and numerous depressions. The median 
ridge, with the highest tubercles, extends from in front of 
the rhinophores almost to the branchia. There are four 
major tubercles on this ridge, one anterior to the rhino- 
phores and three between the rhinophores and branchia. 
The lateral ridges extend from behind the rhinophores to 


either side of the branchia. A few tubercles are scattered 
outside the lateral ridges. The foot (Figure 12) is about 
one-third of the body width. The anterior end is grooved 
with the upper lamina split. The rounded tail is sometimes 
visible when an animal is crawling. Oral tentacles appear 
short and rounded when an animal is at rest; digitiform 


when crawling. 


The rhinophores are long and tapering, with the club 


The Veliger, Vol. 36, No. 1 


angling posteriorly. The club and base are about equal in 
length. The branchia has four gills with numerous large 
pinnae. In one specimen the posterior two gills were split 
about two-thirds of the way up from the base. The bran- 
chial and rhinophore sheaths are low and smooth. The 
anus is long and thin. 

The body is translucent white with numerous irregular 
networks of orange lines extending over most of the dorsal 
surface. These networks are most predominant in the de- 
pressions adjacent to the mid-dorsal ridge, where they may 
fuse, creating pale patches of orange. They may or may 
not join between depressions. The mantle margin is trans- 
lucent white with two fine submarginal orange lines. Often 
these lines attach to the lines on the higher part of the 
dorsum. The apex of the tubercles is orange. The orange 
lines on the body do not extend to the tips of the tubercles, 
thus leaving an unpigmented area surrounding the orange 
tips. The rhinophores are translucent white with brown 
spots, brown lamella, and white tips. The branchia is 
translucent white with brown spots and white tipped brown 
pinnules. The anus is light brown with darker brown spots 
and a white tip. The foot is white, rimmed in orange. The 
oral tentacles have an orange tip. The orange lines toward 
the edge of the dorsum can be seen from below. 

Specimens preserved in alcohol are whitish and have 
retained the brown pigment on the rhinophores and bran- 
chia. A recently preserved specimen retained some yellow 
on the largest tubercles. In some areas, fine white lines 
occur where there were orange lines in the living specimen. 
This is especially noticeable of the submarginal orange 
lines. 


Internal morphology: The internal anatomy appears to 
be the same as that of Halgerda guahan, as well as having 
the transparent visceral sac with sparse brown flecks. 

The radular formulae for 64-mm and 55-mm adult 
specimens were 67 X 61-0-61 and 51 x 71-0-71 respec- 
tively. All teeth except the outer three laterals are simply 
hamate, with a flange on the inner edge. The half row has 
very small inner teeth (Figure 13) gradually increasing in 
size toward the center and decreasing toward the outer 
laterals. The innermost tooth is larger than the outermost 
lateral. A scanning electron micrograph (Figure 14) of the 
55-mm specimen revealed that the three outer laterals are 
flattened plates with irregularities at the apex of the outer 
two. When viewed with a compound microscope (64-mm 
specimen), the innermost of these was smooth; the pen- 
ultimate was denticulate with one large thumblike denticle 
on the inner edge and four to five denticles along the apex; 
the outermost appeared bifid (Figure 14A). 

The general arrangement of the genital system (Figure 
15) is the same as that described for Halgerda guahan, but 
it differs in detail. The hermaphroditic duct connects to 
the ampulla posterior to the genital mass. The broad am- 
pulla appears as a convoluted, somewhat flattened tube at 
the posterior of the prostate and the albumen/mucous 
gland complex. It narrows and enters the genital mass at 


Page 23 


Gere Carlson & Ps Js Hott, 1993 


Explanation of Figures 16 and 17 


Figures 16, 17. Halgerda brunneomaculata sp. nov. Figure 16. 23-mm specimen, Guam, Sella Bay, 4 November 
1972. Figure 17. 16-mm specimen, Guam, Cocos Reef, 3 m depth, 13 September 1970. 


the gland complex, where it joins the prostate gland. The 
whitish prostate gland ensheathes, and folds down under, 
the bursa copulatrix. Two ducts arise adjacent to the area 
where the ampullar duct enters the genital mass. One, the 
uterine duct, makes a loop and extends forward, where it 
enters the bursa copulatrix and the prostate gland. The 
other long, thin duct forms a loop and extends to the 
receptaculum seminis, which it joins posteriorly. The re- 
ceptaculum seminis is embedded in the prostate gland be- 
tween the bursa copulatrix and the female gland complex 
and is partially covered by the vaginal duct. The recep- 
taculum seminis is small and ovoid with a narrow distal 
section. Adjacent to the uterine duct entry into the bursa 
copulatrix is the vaginal mass. The vagina has a large 
glandular layer near its opening. The sinuous vas deferens 
joins the prostate where it covers the bursa copulatrix and 
extends to the large penial sac, which opens into a common 
vestibule with the vagina. The penis and vagina are not 
muscularly connected. A broad extension from the female 
gland mass leads to the genital opening, where it terminates 
in the oviduct. The common opening through the body 
wall for the vagina, penis, and oviduct is lined with dark 
spotted, longitudinal folds. 

Discussion: Halgerda malesso can be compared with H. 
aurantiomaculata (Allan, 1932) and H. terramtuentis Bertsch 
& Johnson, 1982, both white, orange-marked, tuberculate 
species. Externally, H. malesso lacks the colored mantle 
margin as well as the color on the ridges between tubercles 
of these two species. It also differs from H. terramtuentis 
in that the tubercles are capped in orange rather than 
white. All three species have a large penial sac and glan- 
dular structures on the vaginal duct, although the relative 
shape of the duct varies. WILLAN & BRODIE (1989) de- 
scribed folds in the vagina of H. awrantiomaculata, whereas 
in H. malesso folds are found only in the body wall. 

The specific name malesso is the Chamorro name of 
the village in southern Guam where most of the specimens 
have been found. 


Halgerda brunneomaculata 


Carlson & Hoff, sp. nov. 
(Figures 16-21) 


Specimens: Since 1969, 40 specimens of Halgerda brun- 
neomaculata have been found on Guam and two on Sari- 
gan in the Northern Mariana Islands. All but one specimen 
were found at a depth of 3 m or greater, the deepest being 
21 m. The average length of those measured was 13 mm, 
the longest was 23 mm. 


Type material: Holotype (13 mm), Bishop Museum, Ho- 
nolulu, BPBM 209918, 4 m depth, Bile Bay, Guam, 29 


Figure 18 


Halgerda brunneomaculata sp. nov., ventral view, 13-mm spec- 
imen. 


Page 24 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 19 and 20 


Figures 19, 20. Halgerda brunneomaculata sp. nov. Figure 19. Scanning electron micrograph of innermost lateral 
teeth, 23-mm specimen. Figure 20. Camera lucida drawing of outermost lateral teeth, 13-mm specimen. Scale = 


10 um. 


September 1990, Carlson and Hoff. Paratypes (11, 12 mm) 
Bishop Museum, Honolulu, BPBM 209919, 9 m depth, 
Toguon Bay, Guam, 16 April 1972, Carlson and Hoff. 


Material dissected: 1 specimen, 23 mm, Sella Bay, Guam, 
Carlson and Hoff, 4 November 1972; 1 specimen, 13 mm, 
2 m depth, Bile Bay, Guam, Carlson and Hoff, 11 January 
1987; 1 specimen 13 mm, 18 m depth, Bile Bay, Guam, 
Carlson and Hoff, 27 June 1991. Radulae of 23-mm and 
13-mm specimens were used for scanning electron mi- 
crography. 


External morphology (Figures 16, 17): H. brunneo- 
maculata is elongate-ovate. A 16-mm specimen was about 
4 mm in width. The dorsum is marked by a pattern of 
low ridges. The ridges form a series of irregular polygons 
on either side of the midline, sometimes partially crossing 
it. The ridges are slightly higher at their points of juncture, 
but tubercles are not present. The foot (Figure 18) is 
relatively broad and about two-thirds the width of the 
animal. As with the preceding two species, the anterior of 
the foot has a transverse groove. The broad, rounded tail 
extends beyond the posterior mantle edge. The oral ten- 
tacles are digitiform. 

The rhinophores are lamellate for approximately half 
of their length, with the broadest lamellate part being about 
the same width as the heaviest part of the base. There is 
a slight conical tip that is most noticeable in smaller spec- 
imens. Only one specimen showed posterior angulation of 
the club. The branchia is made up of four pinnate branch- 
es. On one specimen, the tip of the two anterior branches 


was divided. Both rhinophores and branchia have a smooth 
low sheath. 

The ground color of Halgerda brunneomaculata is a 
pale translucent yellow. The ridges are marked with a 
darker opaque yellow, which becomes less intense toward 
the mantle edge and terminates in a series of dots rather 
than a solid line. On one 13-mm specimen, the body color 
was dark yellow, presenting no contrast between the ridge 
and body color. Most of the depressions formed by the 
ridges have a single, dark brown spot, although a few 
specimens have scattered spots. Irregular brown spots oc- 
cur on the top of the tail and sides of the foot. A line of 
brown spots occurs at the juncture of the mantle and foot. 
The viscera, as viewed through the dorsal surface, appears 
dark in some specimens and light in others. The rhino- 
phores are translucent white with dark brown lateral stripes. 
The branchia is translucent white with a dark brown stripe 
on the upper side of the rachis. The rhinophore and bran- 
chial sheaths are unmarked. 

Specimens preserved in alcohol vary from pale yellow 
to tan. None of the yellow on the ridges is retained. The 
brown spots and brown lines on the rhinophores and bran- 
chia are retained in some specimens and almost completely 
lost in others. Some of the brown pigment that is retained 
comes off easily when the specimen is handled, a char- 
acteristic also noted by BASEDOW & HEDLEY (1905:152) 
in Halgerda graphica. 


Internal morphology: The general arrangement is similar 
to that described above for Halgerda guahan and H. ma- 


Cw Carlson sak yy Hott, 1993 


lesso, with one major exception. In the preceding two 
species, the main component of the genital system that is 
visible when the animals are opened dorsally is the pros- 
tate-covered bursa copulatrix. The genital system of H. 
brunneomaculata is twisted about 90 degrees to the left, 
which hides the bursa copulatrix under part of the female 
gland mass and digestive and buccal organs, leaving part 
of the female gland mass visible. 

For two 13-mm and one 23-mm adult specimens, the 
radular formulae were 37 X 30-—32:0:30-32, 48 x 35-0: 
35, and 51 x 29-0-29 respectively. All except the outer five 
teeth are simply hamate with a flange on the inner edge. 
In the 13-mm specimen, the inner five teeth (Figure 19) 
were comparatively small and gradually increased in size. 
Teeth six through 12 increased rapidly, and then the re- 
maining laterals increased gradually to the largest teeth 
near the outer end of the half row. The innermost lateral 
was smaller than the outermost lateral. The outer five teeth 
(Figure 20) were small, flattened, and apically pectinate. 
The innermost of these small teeth had a large pectinate 
denticle on its inner edge. Scanning electron micrographs 
of the outermost lateral teeth were not successful because 
the pectinations folded over during dehydration. 

As noted above, the genital mass of Halgerda brunneo- 
maculata, in situ, appears quite different from that of H. 
guahan and H. malesso because of the orientation to the 
left. Otherwise the relationship of the parts of the system 
is much the same (Figure 21). The small hermaphroditic 
duct connects to the ampulla ventrally at the posterior of 
the genital mass. The broad, somewhat flattened, ampulla 
has a large fold, then narrows before entering the albu- 
men/mucous gland complex. The small uterine duct arises 
anterior to the entry of the ampullar duct and extends to, 
and connects with, the bursa copulatrix. The large prostate 
narrows where it folds over to partially enclose the small 
bursa copulatrix. The subovoid receptaculum seminis, 
which is almost as large as the bursa copulatrix, is partially 
embedded in the prostate on one side and lies against the 
bursa copulatrix on the other. It is joined to the uterine 
duct by a short, thin tube. The uterine duct gives the 
appearance of winding over the surface of the bursa cop- 
ulatrix and it exits as the vaginal duct, near the area where 
the narrow part of the prostate folds over the bursa cop- 
ulatrix. This vaginal duct is quite sinuous and broadens 
to form the vagina. The sinuous vas deferens exits from 
the narrowest part of the prostatic fold and leads to the 
elongate penial sheath, which joins the vagina before reach- 
ing the opening through the body wall. A large extension 
from the female gland mass, the oviduct, is adjacent to the 
penis and vagina, where the common opening is situated. 
This opening is lined with longitudinal folds. 


Discussion: Only one other species of Halgerda has been 
described that has a pale yellow ground color, H. formosa 
Bergh, 1880, the type species of the genus. The original 
color notes from Dr. Koerbl state, “gelblichweiss mit or- 


1mm 
Figure 21 


Halgerda brunneomaculata sp. nov. Reproductive system: al, 
albumen gland; am, ampulla; bc, bursa copulatrix; bw, body wall; 
mu, mucous gland; p, penis; pr, prostate; rs, receptaculum sem- 
inis; ud, uterine duct; vd, vas deferens; vg, vagina. 


angegelben Streifen und schwarzen Punkten am Ricken, 
sowie mit schwarzen Rhinophorien” (BERGH, 1880a:191). 
When Bergh worked on the preserved animal he found 
only one black spot and also reported a black band on the 
midline of the tail. We assume that much of the dark 
pigmentation had been lost in the preserved animal Bergh 
examined, as is common with many of our specimens. 
Externally, 1. formosa and H. brunneomaculata appear 
to be similar in terms of body color, darker ridge coloration, 
and the presence of dark spots. The main differences are 
the presence of the dark band on the tail of H/. formosa and 
the lack of dark pigmentation on the rhinophoral base. 
The latter could be from loss of pigmentation in preser- 
vative. Internally, Bergh describes a chocolate-brown vis- 
ceral sac, whereas that for H. brunneomaculata is trans- 
lucent with sparse brown flecks. The oral tube, spotted in 
H. formosa, is unmarked in H. brunneomaculata. The 
number of pectinate laterals is different in the two species: 
two for H. formosa and five for H. brunneomaculata. The 
denticles on the laterals are also much shorter in H. formosa 
than in H. brunneomaculata. Bergh described H. formosa 
as having a bladderlike enlarged vagina with longitudinal 
folds, whereas H. brunneomaculata has a narrow vagina 
and folds are found only in the genital opening through 
the body wall. 

BERGH (1889) described white animals from Mauritius 
also as Halgerda formosa. These animals had yellow ridges 


Page 26 


The Veliger, Vol. 36, No. 1 


and dark spots. Externally they differed from the 1880 7. 
formosa in basic body color, presence of tubercles, and the 
absence of a dark band on the tail. At the present time we 
believe that BERGH’s (1889) H. formosa is probably a dif- 
ferent species. 

The name brunneomaculata was chosen because of the 
dark brown spots present on the animal’s mantle and body. 


DISCUSSION 


In the course of preparing this paper we discovered several 
elements that we feel should be taken into consideration 
in further work on the Halgerda. 

A mid-dorsal pattern with four major points of juncture, 
one in front of the rhinophores and three between rhino- 
phores and branchia, is found in all three animals described 
in this paper. This configuration is not always clearly seen 
in Halgerda brunneomaculata. The six undescribed spe- 
cies in our collection have the same pattern. For those 
species that have a color pattern that does not follow the 
ridges, the major midline points are most obvious in the 
preserved specimens. In tuberculate species, the major tu- 
bercles arise at the points of juncture. 

BERGH (1880b) discussed this pattern for Halgerda tes- 
sellata as did ALLAN (1932) and WILLAN & BRODIE (1989) 
for H. aurantiomaculata. This same pattern appears in 
other Halgerda species, though generally it is not discussed 
in the text, but appears in the figures or plates accom- 
panying an article. Some examples are found in BERGH 
(1905:pl. 2, fig. 4a) for H. elegans Bergh, 1905; BERGH 
(1889:pl. 84, fig. 3) for H. “formosa”; BERTSCH & JOHNSON 
(1981:46-47) for H. terramtuentis; ELIOT (1904:pl. 34, fig. 
1) and GOSLINER (1987:68, fig. 88) for H. wasinensis Eliot, 
1904; and LIN (1975:pl. 2, fig. 7) for H. xishaensis Lin, 
1975: 

The three new species described in this paper have a 
very noticeable flange on the inner edge of all but the 
outermost lateral teeth. BERGH (1880a) also noticed a flange 
when he described Halgerda formosa, as did WILLAN & 
BRODIE (1989) in their work on H. aurantiomaculata. If 
the presence of the flange is not recognized, it can cause 
an interpretation of the teeth that gives a far greater an- 
gulation than actually occurs. 

The three yellowish Halgerda (H. formosa, H. tessellata, 
and /7/. brunneomaculata) so far described have pectinate 
outer laterals. This feature is not limited to the yellowish 
species because it is also found in H. elegans Bergh, 1905, 
and H. xishaensis Lin, 1975. What appears to be unique 
among the yellow forms is the large denticle that occurs 
on the inner edge of the innermost of the pectinate teeth. 


ACKNOWLEDGMENTS 
We would like to thank Dr. Terrence Gosliner of the 
California Academy of Sciences, who graciously offered to 


furnish SEM plates and Ignacio S. “Buck” Cruz, Mayor 
of Malesso, for his support during preparation of this 


article. This paper is contribution No. 323 from the Uni- 
versity of Guam Marine Laboratory. 


LITERATURE CITED 


ALLAN, J. K. 1932. Australian Nudibranchiata. Australian 
Zoologist 7(2):87-105. 

BASEDOW, H. & C. HEDLEY. 1905. South Australian nudi- 
branchs, and an enumeration of the known Australian spe- 
cies. Transactions, Proceedings & Reports, Royal Philo- 
sophical Society South Australia 29:134-160. 

BERGH, R. 1880a. Beitrage zue Kenntniss der japanischen Nu- 
dibranchien I. Verhandlungen der Zoologish-botanischen 
Gesellschaft in Wien 30:155-200. 

BERGH, R. 1880b. Malacologische Untersuchungen. Jn: Reisen 
im Archipel der Philippinen von Dr. Carl Gottfried Semper. 
Zweiter Theil. Wissenschaftliche Resultate. Band 2, Theil 
4, Heft 1:1-78. 

BERGH, R. 1881. Beitrage zur Kenntniss der japanischen Nu- 
dibranchien II. Verhandlungen der Zoologisch-botanischen 
Gesellschaft in Wien 31:219-54 [contains plates for BERGH, 
1880a]. 

BERGH, R. 1889. Malacologische Untersuchungen. /n: Reisen 
im Archipel der Philippinen von Dr. Carl Gottfried Semper. 
Zweiter Theil. Wissenschaftliche Resultate. Band 2, Theil 
3, Heft 16, 2 Halfte:815-872. 

BERGH, R. 19065. Die Opisthobranchiata der Siboga Expedi- 
tion. Siboga Expedition Reports 50:1-248. 

BERTSCH, H. & S. JOHNSON. 1981. Hawaiian Nudibranchs. 
Oriental Publishing Co.: Honolulu. 112 pp. 

BERTSCH, H. & S. JOHNSON. 1982. Three new species of dorid 
nudibranchs (Gastropoda: Opisthobranchia) from the Ha- 
waiian Islands. The Veliger 24(3):208-218. 

Burn, R. 1975. Appendix: a list of the dorid nudibranchs of 
Australia (Gastropoda, Opisthobranchia). Pp. 514-517. In: 
T. E. Thompson, Dorid nudibranchs from eastern Australia 
(Gastropoda, Opisthobranchia). Journal of Zoology 176(4): 
477-517. 

Carson, C. H. & P. J. Horr. 1973. Some unshelled shells 
of Guam. Guam Recorder 3(2):5-8. 

Euiot, C. N. E. 1903 [1904]. On some nudibranchs from East 
Africa and Zanzibar. Part III. Proceedings of the Zoological 
Society of London 2:354-385. 

ELIoT, C. N. E. 1905. On some nudibranchs from the Pacific, 
including a new genus, Chromodoridella. Proceedings of the 
Malacological Society of London 6(4):229-238. 

GOSLINER, T. 1987. Nudibranchs of Southern Africa. Sea Chal- 
lengers: Monterey. 

JOHNSON, S. & L. M. BOUCHER. 1983. Notes on some Opis- 
thobranchia (Mollusca: Gastropoda) from the Marshall Is- 
lands, including 57 new records. Pacific Science 37(3):251- 
291. 

Lin, G. 1975. Opisthobranchia from the inter-tidal zone of 
Xisha Islands, Guangdong Province, China. Studia Marina 
Sinica 10:141-154. 

RuDMAN, W. B. 1978. The dorid opisthobranch genera Hal- 
gerda Bergh and Sclerodoris Eliot from the Indo-West Pacific. 
Zoological Journal of the Linnean Society 62(1):59-88. 

WILLAN, R. C. & G. D. BRopiE. 1989. The nudibranch Hal- 
gerda aurantiomaculata (Allan, 1932) (Doridoidea: Doridi- 
dae) in Fijian waters. The Veliger 32(1):69-80. 

WILLAN, R. C. & N. COLEMAN. 1984. Nudibranchs of Aus- 
tralasia. Australasian Marine Photographic Index: Sydney. 


56 pp. 


The Veliger 36(1):27-35 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


New Species and Records of Lepetodrilus 


(Vetigastropoda: Lepetodrilidae) 


from Hydrothermal Vents 


JAMES H. McLEAN 


Los Angeles County Museum of Natural History, 
900 Exposition Boulevard, Los Angeles, California 90007, USA 


Abstract. Two new species of Lepetodrilus are described from the east Pacific hydrothermal vents: 
L. tevnianus from the East Pacific Rise near 11°N, where it is associated with the vestimentiferan 
Tevnia jerichonana Jones, 1985, and L. corrugatus from the Juan de Fuca Ridge, known from a single 
specimen, its tentative association being directly on the sulfide chimney. Lepetodrilus elevatus McLean, 
1988, previously understood to be widely distributed at the east Pacific vents, is confirmed from the 
Mariana vents, where it apparently lives away from the vestimentiferans with which it is associated in 
the eastern Pacific. It is the only molluscan species known from both the eastern Pacific and mid- Pacific 
vents. Lepetodrilus fucensis McLean, 1988, previously known from the Explorer and Juan de Fuca 
Ridges, is reported at the Gorda Ridge. Lepetodrilus guaymasensis McLean, 1988, previously known 
from five specimens, is now known from 127 additional specimens from the type locality. 


INTRODUCTION 


Lepetodrilus McLean, 1988, family Lepetodrilidae, super- 
family Lepetodrilacea, is unique among the genera of ar- 
chaeogastropod limpets associated with hydrothermal vents 
in having three pairs of epipodial tentacles and a right 
cephalic-epipodial penis. Anatomy was described in a com- 
panion paper by FRETTER (1988). Relationships of the 
superfamily have also been discussed by HASZPRUNAR 
(1988), who assigned it to the suborder Vetigastropoda. 

Six species of Lepetodrilus were initially described. In 
this paper I add the descriptions of two more species, and 
give range extensions or additional records for three of the 
original species. The new species and records of previously 
described species add new limits to the expression of mor- 
phological character states and new parameters to the un- 
derstanding of biological associations and the capacity for 
long distance dispersal in the genus. These topics are treat- 
ed in the discussion section. 


MATERIALS anp METHODS 


All specimens reported here were collected by expedition 
members on various cruises to hydrothermal vent sites that 
employed the deep-submersible Alvin or other submers- 
ibles. Limpet specimens were collected with the mechanical 
arm of the submersible in the course of collecting substrate 


samples or general collecting of all organisms. Specimens 
were preserved on reaching the surface and were originally 
fixed for 24 hr in 10% formalin-seawater buffered with 
sodium borate, washed in fresh water, and transferred to 
70% ethanol. 

Radulae were extracted from preserved specimens after 
dissolution of tissues with room temperature 10% NaOH 
for 48 hr, washed in distilled water, dried from a drop of 
water on a stub having a thin smear of rubber cement, 
and coated with gold palladium for SEM examination. 
Repositories of type and other material are the Los Angeles 
County Museum of Natural History (LACM), the United 
States National Museum (USNM), and the Museum Na- 
tional d’Histoire Naturelle, Paris (MNHN). 


SYSTEMATIC DESCRIPTIONS 
Order Archaeogastropoda Thiele, 1925 
Suborder Vetigastropoda Salvini-Plawen, 1980 
Superfamily LEPETODRILACEA McLean, 1988 
Family LEPETODRILIDAE McLean, 1988 


Lepetodrilus McLean, 1988 


Lepetodrilus MCLEAN, 1988:6. Type species: L. pustulosus 
McLean, 1988. 


The Veliger, Vol. 36, No. 1 


Table 1 


Lepetodrilus teunianus. Measurements and disposition of holotype and paratype specimens. 


Page 28 
Length Width 
(mm) (mm) 
LACM 2254 9.5 7.9 
USNM 859484 8.9 7.8 
USNM 859484 8.8 7.6 
LACM 2255 8.1 7.0 
LACM 2255 6.9 5.8 


Lepetodrilus species are diagnosed by differences in shell 
profile, sculpture, penial morphology, and radular mor- 
phology, particularly that of the rachidian and first lateral 
teeth. Each of the previously described species, as well as 
the two species described here, can be recognized on rad- 
ular characters alone. 


Lepetodrilus teunianus McLean, sp. nov. 
(Figures 1-10) 


Description: Shell (Figures 1-3) moderately large for ge- 
nus (maximum length 9.5 mm). Outline of aperture oval, 
anterior end markedly tapered to produce faintly angulate 
anterior tip. Margin of aperture not in same plane, ends 
raised relative to sides. Anterior slope convex except con- 
cave near margin; lateral and posterior slopes concave. 
Apex at one-quarter shell length from posterior margin, 
below highest elevation of shell, displaced slightly to right, 
right side of protoconch remaining visible. Periostracum 
moderately thick, light yellow-brown, turned in at shell 
edge. Early shell to 1 mm length devoid of sculpture; single 
mid-dorsal rib on anterior slope arising first, remaining 
stronger than all other ribs; fine primary ribs arising at 
shell length of 1-3 mm; secondary ribs arising at shell 
length of about 4 mm, quickly assuming strength of pri- 
mary ribs. Large specimens with 6 ribs/mm at margin. 
Ribs minutely beaded to correspond to growth lines, re- 
maining strong at later stages of growth. Interior surface 
glossy, opaque, with scattered white discolorations. Pos- 
terior half of shell interior with faintly angulate curved 
ridge outside of muscle scar. Muscle scar horseshoe-shaped, 
not deeply marked, positioned on inner surface of curved 
ridge midway between margin and midline; scar relatively 
broad, broadest anteriorly, narrow posteriorly. Apical pit 
prominent, not filled by deposition of callus. 

Dimensions of holotype: Length 9.5, width 7.9, height 2.8 
mm. 

External anatomy (Figures 4-6): Typical for genus. Epi- 
podial tentacles three pairs, one lateral pair and two pos- 
terior pairs, each with cylindrical tip and triangular base. 
Cephalic tentacles long, encircled laterally and ventrally 
by epipodial folds, eyes lacking. Oral disk broad, mouth 
Y-shaped. Anterior of foot with double edge, marking 
opening of pedal gland. Mantle edge with two folds, inner 


Height 

(mm) Remarks 
2.8 Holotype, female (Figures 1-5) 
2.8 Intact female 
Dil: Intact female 
— Female, shell broken, radula 

preparation (Figures 7-10) 

2.0 Male, shell deformed (Figure 6) 


fold smooth to extend under periostracum, edge of outer 
fold finely divided. Penis of male (Figure 6) flaplike, its 
origin on right ventral neck. Mantle cavity and ctenidium 
typical for genus, ctenidium projecting above head in ven- 
tral view (Figure 5). 

Radula (Figures 7-10): Rhipidoglossate; laterals five 
pairs, cusp rows of first and second laterals forming in- 
verted-U; marginals numerous, cusp rows descending. Ra- 
chidian broad at base, shaft shorter than that of laterals, 
rachidian with very long, tapered central cusp, edges with 
about six sharply pointed denticles; shaft of rachidian with 
projecting lateral extension fitting against edge of first 
lateral. First lateral large and complex, curved overhang 
broad at its distal edge. Inner edge of shaft of first lateral 
continuous with main cusp, projecting so that it appears 
to be a long pointed denticle like that of rachidian; outer 
edge of shaft with hooked projection that articulates with 
shaft of second lateral. Overhanging edge of first lateral 
with about eight long, unseparated denticles on inner edge, 
followed by a major denticle and at least three shorter 
denticles on outer edge. Second, third, and fourth laterals 
similar to each other, cusps long, tapered, with serrate 
edges; fifth lateral broader. Marginal teeth similar to each 
other, tips with numerous, deeply cut serrations. 


Type locality: On vestimentiferan Teunia jerichonana 
Jones, 1985, living on basalt cliff overhanging low tem- 
perature venting water, East Pacific Rise near 11°N 
(10°56.3'N, 103°41.4’W), 2536 m. 


Type material: 5 specimens (4 females, 1 male) from the 
type locality, recovered from washings of specimens of 
Tevnia jerichonana, Alvin dive 1986, 8 March 1988. Re- 
ceived from Cindy Lee Van Dover. Holotype, LACM 
2254; 2 paratypes, LACM 2255; 2 paratypes, USNM 
859484. Dimensions and disposition of all specimens are 
given in Table 1. 


Remarks: Lepetodrilus teunianus is easily distinguished 
from the other species of Lepetodrilus in characters of the 
shell, penial morphology, and radula. The shell most re- 
sembles that of L. pustulosus, but has the strong anterior 
rib, is broader, has a more angulate anterior (dorsal view), 
and lacks the diverging curves in the alignment of the beads 
on the radial ribs, as well as lacking the two supporting 


J. H. McLean, 1993 


Page 29 


Explanation of Figures 1 to 6 


Figures 1-6. Lepetodrilus teuntianus McLean, sp. nov. Alvin dive 1982, East Pacific Rise near 11°N, 2536 m. 
Anterior at top in vertical views. Figures 1-3. Holotype shell, LACM 2254. Length 9.5 mm. Exterior, interior, 
and left lateral views. Figures 4, 5. Holotype body (female). Dorsal and ventral views. Figure 6. Paratype, male 


body attached to shell, LACM 2255. Length 6.9 mm. 


ridges below the apex on the posterior slope of that species. 
The flat, non-elbowed morphology of the penis is char- 
acteristic. The radula of L. teunianus is unlike that of any 
other species of Lepetodrilus. The rachidian is unique in 
having a very long cusp and large, conspicuous flanks to 
the shaft; the first lateral is unique in its prominent inner 
edge of the shaft. 

The significance of the association of this species with 
a vestimentiferan other than Riftza pachyptila is treated 
further in the discussion section. 


Etymology: The name tevnianus, means of Tevnia, the 
vestimentiferan on which this species lives. 


Lepetodrilus corrugatus McLean, sp. nov. 
(Figures 11-16) 


Description (based on single female specimen): Shell 
(Figures 11-13) medium-sized for genus (length 6.1 mm). 
Outline of aperture oval, anterior end slightly narrower 
than posterior. Margin of aperture not in same plane, ends 
raised relative to sides. Anterior slope convex, lateral slopes 
flat, posterior slope convex below apex. Apex at one-eighth 


shell length from posterior margin, below highest elevation 
of shell, apex displaced slightly to right; protoconch surface 
eroded, not visible on right side. Periostracum moderately 
thick, light greenish-brown, turned in at shell edge. Early 
shell to 1 mm length devoid of sculpture. Mature sculpture 
dominated by about six irregularly formed concentric 
swellings, producing a wrinkled appearance; additional 
concentric sculpture of fine growth lines on periostracum. 
Radial sculpture of low ribs, strongest posteriorly and 
laterally, interspaces broader than ribs. Ribs only faintly 
beaded to correspond to growth lines. Interior surface 
opaque, chalky (probably etched by preservation fluids), 
showing the coarse, irregular concentric sculpture of the 
exterior. Posterior half of shell interior with strongly an- 
gulate, curved ridge outside of muscle scar. Muscle scar 
horseshoe-shaped, not deeply marked, positioned on inner 
surface of curved ridge midway between margin and mid- 
line; scar relatively broad, broadest anteriorly, narrow pos- 
teriorly. Apical pit prominent, not filled by deposition of 
callus. 

Dimensions of holotype: Length 6.1, width 4.7, height 2.2 
mm. 


ly Ae 


The Veliger, Vol. 36, No. 1 


_S 


Explanation of Figures 7 to 10 


Figures 7-10. Lepetodrilus teunianus McLean, sp. nov. SEM views of radula of paratype, LACM 2255. Figure 
7. Full width of ribbon. Scale bar = 40 um. Figure 8. Rachidian and first three laterals. Scale bar = 10 um. Figure 
9. Rachidian and adjacent edge of first lateral. Scale bar = 4 um. Figure 10. Detail of serrations on marginal teeth. 


Scale bar = 10 um. 


External anatomy (Figure 14): Typical for genus. Epi- 
podial tentacles three pairs, one lateral pair and two pos- 
terior pairs, each with cylindrical tip and triangular base. 
Cephalic tentacles short (preserved condition), encircled 
laterally and ventrally by epipodial folds, eyes lacking. 
Oral disk broad, mouth Y-shaped. Foot anterior with dou- 
ble edge, marking opening of pedal gland. Mantle edge 
with two folds, edge of outer fold smooth to extend under 
periostracum, edge of inner fold finely divided. Mantle 
cavity and ctenidium typical for genus, ctenidium not pro- 
jecting above head in ventral view (Figure 14). 

Radula (Figures 15, 16): Rhipidoglossate; lateral teeth 
five pairs, cusp rows of first and second laterals forming 
inverted-U; marginals numerous, cusp rows descending. 
Rachidian broad at base, shaft shorter than that of laterals, 


with tapered central cusp, edges with about three sharply 
pointed denticles; shaft of rachidian with projecting lateral 
extension fitting against edge of first lateral. First lateral 
large and complex, shaft broad, curved overhang broader 
distally from rachidian, distal portion bearing about six 
sharp denticles, inner portion with one major and two or 
three minor denticles. Second, third, and fourth laterals 
similar to each other, cusps long, tapered, edges not serrate; 
fifth lateral with deeply serrate edges. Marginal teeth sim- 
ilar to each other, tips with numerous, deeply cut serra- 
tions. 


Type locality: Heinecken Hollow, Middle Valley, Juan 
de Fuca Ridge, west of Washington (48°25.8'N, 
128°40.9'W), 2420 m. 


J. H. McLean, 1993 


Page 31 


a 


Explanation of Figures 11 to 16 


Figures 11-16. Lepetodrilus corrugatus McLean, sp. nov. Alvin dive 2252. Middle Valley, Juan de Fuca Ridge off 
Washington, 2420 m. Anterior at top in vertical views. Figures 11-14. Holotype, LACM 2256. Length 6.1 mm. 
Exterior, interior, right lateral, and body (female) before detachment from shell. Figures 15, 16. SEM views of 
radula of holotype. Figure 15. Width of ribbon. Scale bar = 20 um. Figure 16. Rachidian and lateral teeth. Scale 


bar = 10 um. 


Type material: 1 specimen (female) from the type locality, 
recovered from sample containing broken pieces of sulfide 
chimney, Alvin dive 2252, 5 August 1990. Recognized 
during sample sorting by K. Wilson and forwarded by 
Verena Tunnicliffe. Holotype, LACM 2256. The holotype 
body is intact except for removal of the radula. 


Remarks: Lepetodrilus corrugatus is known from a single 


female specimen. The morphology of the penis, an im- 
portant external character in members of this genus, is 
therefore unknown. Attempts by K. Wilson to locate ad- 
ditional specimens in samples from the Middle Valley site 
on the Juan de Fuca Ridge have been unsuccessful (V. 
Tunnicliffe, personal communication). The type locality 
is a new site on the northern Juan de Fuca Ridge for 
which there are faunal and structural differences from 


Page 32 


other sites that will be described by V. Tunnicliffe. The 
species is described from a single specimen in order to 
update knowledge of the family. 

Lepetodrilus corrugatus differs from its congeners in 
both shell and radular characters. It is the only species 
having the sculpture dominated by deep, irregular con- 
centric undulations. In general proportions and sculpture 
it is most similar to L. pustulosus. Differences, in addition 
to the corrugate sculpture, are its more oval outline, more 
posterior apex, coarser radial ribs, and lack of the two 
strong radial ribs that subtend the apex. It differs from L. 
elevatus in its sculpture and its broader anterior outline, 
as well as radular characters. 

The radula of Lepetodrilus corrugatus requires com- 
parison with that of L. pustulosus and L. fucensis, both of 
which have similarly proportioned first lateral teeth. The 
rachidian of L. corrugatus differs from that of L. pustulosus 
in having fewer serrations and not having the concave 
depression on the overhanging surface; details in the place- 
ment of cusps of the elongate first lateral also differ. Similar 
differences separate the radulae of L. corrugatus from that 
of L. fucensis; the latter species also differs in having a 
marked concavity on the overhanging surface of the ra- 
chidian. 

The occurrence of this species on the sulfide chimney 
microhabitat is unique in the genus and needs to be verified 
by the collection of further specimens. It occurs sympat- 
rically with the abundant species Lepetodrilus fucensis. 


Etymology: The name corrugatus is a Latin adjective 
meaning “wrinkled” or “ridged,” with reference to the 
dominant shell sculpture. 


Lepetodrilus elevatus McLean, 1988 
(Figures 17-25) 


Lepetodrilus elevatus MCLEAN, 1988:11, figs. 5,5, 36-44; 
McLEan, 1990a:84. 

Lepetodrilus cf. elevatus: HESSLER & LONSDALE, 1991a:190; 
HESSLER & LONSDALE, 1991b:171. 


New records: 29 specimens from Alvin dive 1837, Burke 
Field vents, Mariana Trough spreading center (18°10.9’N, 
144°43.2’E), 3660 m, 28 April 1987. Received from Robert 
R. Hessler. Disposition: 14 specimens LACM 146884; 10 
specimens USNM 882027; 5 specimens MNHN. 

Nine specimens from Alvin dive 1843, Alice Springs 
vents, Mariana Trough spreading center (18°12.6'N, 
144°42.4'E), 3640 m, 4 May 1987. Received from Robert 
R. Hessler. Disposition: 5 specimens LACM 146885; 4 
specimens USNM 882028. 


Remarks: The presence of this species at the Mariana 
Trough vents has previously been reported by MCLEAN 
(1990a) and by HESSLER & LONSDALE (1991a, b), but 
detailed commentary and illustrations have not been given. 
Material from the Mariana Trough (Figures 17-25) 
matches that illustrated by MCLEAN (1988) for specimens 


The Veliger, Vol. 36, No. 1 


of the typical subspecies Lepetodrilus elevatus elevatus from 
the East Pacific Rise at 21°N. All specimens of the present 
material have surficial markings on the periostracum made 
by an unknown organism, but this does not penetrate the 
periostracum and has no significance for taxonomic com- 
parison. Specimens originally described from the Gala- 
pagos Rift were consistently lower in profile (at two-thirds 
the height of the typical subspecies) and were given the 
subspecific name L. elevatus galriftensis, but the present 
material has the high profile of the typical subspecies. All 
specimens of the material from the Mariana Trough ap- 
pear to be famale, none having the broad triangular penis 
illustrated by MCLEAN (1988:pl. 6, fig. 39). The signifi- 
cance of this is unknown and needs to be further investi- 
gated. Genetic (electrophoretic) evidence that the two pop- 
ulations represent the same species would also be of interest. 


Lepetodrilus guaymasensis McLean, 1988 


Lepetodrilus guaymasensis MCLEAN, 1988:16, figs. 15, 16, 
66-74. 


New records: 98 small to medium-sized specimens (not 
sexed) from Alvin dive 1613, Guaymas Basin (27°00.5’N, 
111°24.6'W), 2007 m, 5 August 1985. Received from Mer- 
edith R. Jones. Disposition: 48 specimens LACM 146886; 
30 specimens USNM 882029; 20 specimens MNHN. 

Twenty-nine specimens (21 male, 8 female) from Alvin 
dive 1615, Guaymas Basin (27°00.5'N, 111°24.6’W), 2000 
m, 7 August 1985. Received from Meredith R. Jones. 
Disposition: 13 specimens LACM 146887; 10 specimens 
USNM 882030; 6 specimens MNHN. 


Remarks: Lepetodrilus guaymasensis was described origi- 
nally from five specimens; the 127 specimens reported here 
from the 1985 expedition to the Guaymas Basin (Fred 
Grassle, Chief Scientist) are a significant increase in the 
number known. Both samples were recovered from wash- 
ings of Riftia pachyptila. 


Lepetodrilus fucensis McLean, 1988 


Lepetodrilus fucensis MCLEAN, 1988:18, figs. 17-20, 75-83; 
McLEAaNn, 1990b:496. 


New records: 15 specimens (9 male, 6 female) from Sea 
Cliff dive 764, Escanaba Trough, Gorda Ridge (41°00’N, 
127°29'W), 3200-3250 m, 3 September 1988. Received 
from Robert R. Hessler. Disposition: 7 specimens LACM 
146888; 5 specimens USNM 882031; 3 specimens MNHN. 

Twenty-three specimens (12 male, 11 female) from Al- 
vin dive 2036, Escanaba Trough, Gorda Ridge (41°00.4’N, 
127°29.3'W), 3240 m, 6 June 1988. Received from Cindy 
Lee Van Dover. Disposition: 9 specimens LACM 146889; 
8 specimens USNM 882032; 6 specimens MNHN. 


Remarks: This species, which is abundantly known from 
the Explorer and Juan de Fuca Ridges, was reported by 
MCLEAN (1990b) from Escanaba Trough on the Gorda 
Ridge. Disposition of the material is given here. As re- 


J. H. McLean, 1993 Page 33 


Explanation of Figures 17 to 25 


Figures 17-25. Lepetodrilus elevatus McLean, 1988. Alvin dive 1837. Burke Field, Mariana vents, 3660 m. Anterior 
at top in vertical views. Figures 17-20. LACM 146884. Length 6.8 mm. Figures 17-20. Exterior, interior, right, 
and left lateral views. Markings on shell produced by unknown organism. Figures 21-23. Detached body of same 
specimen as in Figures 17-20. Dorsal, ventral, and lateral views. Figures 24, 25. SEM views of radula, LACM 


146884. Figure 24. Rachidian, lateral, and inner marginal teeth. Scale bar = 20 wm. Figure 25. Full width of 
ribbon. Scale bar = 40 um. 


Page 34 


ported initially, there is no known association with vesti- 
mentiferans. A general description of the biotic community 
of the Escanaba Trough was given by VAN DOVER et al. 
(1990). 


DISCUSSION 


The discription of two additional species brings the total 
number of described species of Lepetodrilus to eight. The 
genus remains the most speciose of limpet genera in the 
hydrothermal-vent habitat. Eight of the species are known 
from eastern Pacific vents; one of these species, L. elevatus, 
is also known from the Mid-Pacific Mariana vents (the 
only mollusk with such a distribution). 

Until now, the only association between species of Le- 
petodrilus and vestimentiferans had been with the vesti- 
mentiferan Riftia pachyptila. MCLEAN (1988) reported that 
washings of retrieved specimens of that vestimentiferan 
were highly productive in collecting L. pustulosus, L. ele- 
vatus, L. ovalis, and L. cristatus. Lepetodrilus teunianus is 
the only species yet reported to be associated with the 
vestimentiferan 7eunia jerichonana, a vestimentiferan pre- 
viously reported by JONES (1985) as occurring only at the 
French expedition site at 13°N. Lepetodrilus teunianus is 
yet unknown from 13°N, although its vestimentiferan as- 
sociate is present at that site. Riftia pachyptila was not 
recorded from the type locality of Tevnia jerichonana (Alvin 
dive 1986). The only other Lepetodrilus species occurring 
with L. teunianus was L. elevatus. This pattern of distri- 
bution suggests that L. teunianus depends on the presence 
of Tevnia jerichonana, and that the most abundant species, 
L. elevatus, can be associated with either species of vesti- 
mentiferan, whereas three other species of Lepetodrilus are 
associated only with Riftia pachyptila. 

The two northernmost occurring species, Lepetodrilus 
fucensis, which occurs clustered on hard surfaces near vents 
and chimneys, and L. corrugatus, which is now known 
from a single specimen, but may prove to be associated 
with the hard surface deposits of sulfide chimneys, differ 
from other eastern Pacific species in having no known 
association with vestimentiferans. The physical and bio- 
logical parameters of the sulfide chimney habitat have been 
discussed by TUNNICLIFFE (1990), although the limpets 
were not mentioned. 

Lepetodrilus elevatus, the most broadly distributed spe- 
cies of the genus, is also the most diverse in its substrate 
associations. At the eastern Pacific vents it occurs with two 
different species of vestimentiferans, yet it appears to be 
capable of living away from vestimentiferans, there being 
no reported vestimentiferans at the Mariana Trough. 

FIESSLER & LONSDALE (1991a, b) have recently dis- 
cussed the biogeographic implications of the species known 
from the Mariana Trough and the eastern Pacific. The 
fact that one species of Lepetodrilus has bridged the gap 
seems difficult to explain. However, HESSLER & LONSDALE 
(1991) noted that “two now-extinct portions of the mid- 


The Veliger, Vol. 36, No. 1 


ocean ridge system would have allowed comparatively easy 
interchange 43 and 55 million years ago.” 

In the genus Lepetodrilus the biogeographic affinity be- 
tween the East Pacific Rise and the Juan de Fuca Ridge 
extends only to the generic level, as no species are shared 
between the two systems. Biogeographic affinity of these 
two systems has been treated by TUNNICLIFFE (1988). 

My earlier assessment (MCLEAN, 1988) that the lepe- 
todrilaceans may represent limpet derivatives of unknown 
Paleozoic or Mesozoic archaeogastropods has not been 
challenged nor supported with further evidence. Additional 
arguments in support of the concept that the hydrothermal- 
vent fauna as a whole represents an ancient relict fauna 
have been given by TUNNICLIFFE (1991; in press). A con- 
certed effort to apply the techniques of molecular genetics 
will be necessary to test this hypothesis of antiquity, but 
that is left to future investigators. 


ACKNOWLEDGMENTS 


For providing material of the new species and new records 
reported here I thank: Cindy Lee Van Dover of Woods 
Hole Oceanographic Institution; Verena Tunnicliffe and 
K. Wilson of the University of Victoria, British Columbia; 
Bob Hessler and Michel Boudrias of Scripps Institution 
of Oceanography, Fred Grassle and Rosemarie Petrecca 
of Rutgers University, New Jersey; and Meredith Jones 
of the U.S. National Museum of Natural History. Pho- 
tographs are the work of Bertram C. Draper. SEM work 
was done by C. Clifton Coney, using the CEMMA facility 
of the University of Southern California. For helpful com- 
mentary I thank Anders Waren of the Swedish Museum 
of Natural History, Stockholm, and two anonymous re- 
viewers. 


LITERATURE CITED 


FRETTER, V. 1988. New archaeogastropod limpets from hy- 
drothermal vents; Superfamily Lepetodrilacea. II. Anatomy. 
Philosophical Transactions of the Royal Society of London, 
B, 319:33-82. 

HASZPRUNAR, G. 1988. On the origin and evolution of major 
gastropod groups, with special reference to the Streptoneura. 
Journal of Molluscan Studies 54:367-441. 

HESSLER, R. R. & P. F. LONSDALE. 1991a. Biogeography of 
Mariana Trough hydrothermal vent communities. Deep-Sea 
Research 38:185-199. 

HESSLER, R. R. & P. F. LOMSDALE. 1991b. The biogeography 
of the Mariana Trough hydrothermal vents. Pp. 165-182. 
In: J. Mauchling & T. Nemoto (eds.), Marine Biology, its 
Accomplishment and Future Prospect. Hokusen-sha (Ja- 
pan). 

Jones, M. L. 1985. On the Vestimentifera, new phylum: six 
new species and other taxa, from hydrothermal vents and 
elsewhere. Biological Society of Washington, Bulletin 6:117- 
158. 

McLean, J. H. 1988. New archaeogastropod limpets from 
hydrothermal vents; Superfamily Lepetodrilacea. I. System- 
atic Descriptions. Philosophical Transactions of the Royal 
Society of London, B, 319:1-32. 


J. H. McLean, 1993 


McLean, J. H. 1990a. A new genus and species of neomphalid 
limpet from the Mariana vents, with a review of current 
understanding of relationships among Neomphalacea and 
Peltospiracea. The Nautilus 104(3):77-86. 

McLean, J. H. 1990b. Neolepetopsidae, a new docoglossate 
limpet family from hydrothermal vents and its relevance to 
patellogastropod evolution. Journal of Zoology, London 222: 
485-528. 

TUNNICLIFFE, V. 1988. Biogeography and evolution of hydro- 
thermal-vent fauna in the eastern Pacific Ocean. Proceedings 
of the Royal Society of London, Series B, 233:347-366. 

TUNNICLIFFE, V. 1990. Dynamic character of the hydrothermal 


Page 35 


vent habitat and the nature of sulphide chimney fauna. Prog- 
ress in Oceanography 24:1-13. 

TUNNICLIFFE, V. 1991. The biology of hydrothermal vents: 
ecology and evolution. Annual Review of Oceanography and 
Marine Biology (Margaret Barnes, ed.) 29:319-407. 

TUNNICLIFFE, V. In press. The nature and origin of the modern 
hydrothermal vent fauna. Palaios. 

VAN Dover, C. L., J. F. GRAsSSLE & M. Bouprias. 1990. 
Hydrothermal vent fauna of Escanaba Trough (Gorda Ridge). 
Pp. 285-287. In: G. R. McMurray (ed.), Gorda Ridge: A 
Seafloor Spreading in the United States’ Exclusive Economic 
Zone. Springer-Verlag: New York. 


The Veliger 36(1):36-42 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A Defensive Value of the Thickened 


Periostracum in the Mytiloidea 


by 


E. M. HARPER 


Department of Earth Sciences, Downing St., Cambridge, UK 


AND 


P. W. SKELTON 


Department of Earth Sciences, The Open University, Milton Keynes, UK 


Abstract. 


Laboratory experiments demonstrate the advantages which accrue to epifaunal mussels 


from their possession of a thick periostracum, as a defense against boring predation. Muricid gastropods, 
Nucella lapillus and Morula musiva, displayed a statistically significant preference for boring those valves 
from which the thick periostracal layer had been removed. Although it is possible for muricids to 
penetrate the periostracum it is suggested that this tough, relatively inert, layer is more difficult to 
penetrate than the calcareous parts of the shell. In this respect its defensive value is analogous to that 
of the intra-shell layers of conchiolin reported in certain oysters and Corbuloidea. The thickness of the 
earlier formed periostracum diminishes as the individual ages, either by decay or abrasion, and in most 
cases it is thinnest, or even absent, over the oldest parts of the shell. This may have some bearing on 
the position of most boring activity. As yet it is unclear whether the thickening of the mytilacean 
periostracum was selected for by the evolution of boring predators or whether the defensive value was 
a fortuitous spin off of a non-adaptive or otherwise selected character. 


INTRODUCTION 


The primary function of the molluscan periostracum is 
considered to be one of involvement in shell secretion, either 
as a template onto which the calcareous portion of the shell 
forms (TAYLOR & KENNEDY, 1969) or as a barrier par- 
titioning the extrapallial fluid from the poisoning effects 
of magnesium ions in seawater and contamination by sed- 
iment particles (CLARK, 1976). The sheet may also protect 
the calcareous shell from dissolution in acidic waters; hence 
its extreme development in some freshwater taxa (TEVESZ 
& CARTER, 1980). More recently, some authors have sug- 
gested that the periostracum of some mollusks may have 
a defensive role. WRIGHT & FRANCIS (1984) have -exper- 
imentally shown that the periostracal awns of Modiolus 


modiolus (Linnaeus, 1758) inhibit pedal attachment of the 
boring muricid Nucella lapillus (Linnaeus, 1758) from 
which they infer a defensive value. BOTTJER (1981) ex- 


amined the shells of the cymatiid gastropod Fusitriton or- 
egonensis (Redfield, 1846), finding that areas of the shell 
where the thick hairy periostracum was intact showed 


fewer borings and encrusting epibionts than regions where 
the periostracum had been removed by erosion. This paper 
considers further the defensive value of the mytilid peri- 
ostracum in the deterrence of boring muricid predators. 
The Mytiloidea possess a particularly thick periostracum 
which, despite the ravages of decay and abrasion, is re- 
markably persistent through life. Although there is intra- 
specific variation in the value, initial measurements for 29 
species of byssate mytilaceans show that the intact layer 
always exceeds 20 um in thickness (Harper, unpublished). 
The highest value recorded is for an individual of Cho- 
romytilus chorus at over 400 wm, but for the vast number 
of species the value lies between 20 and 80 um (example 
values include Perna viridis (Linnaeus, 1758), 45 um; Sep- 
lifer virgatus (Wiegmann, 1837), 59 wm; and Mytilus edulis 
(Linnaeus, 1758), showing a wide variation up to 70 um). 
These high values contrast directly with those for a number 
of other epifaunal bivalves, for example oysters and pec- 
tinids, which have extremely thin periostraca (less than a 
micron thick), which is seldom detectable beyond the valve 
margin. Muricid gastropods are well known for their abil- 


E. M. Harper & P. W. Skelton, 1993 


ity to feed on epifaunal bivalves by boring through the 
prey shell to gain access to the flesh beneath. Indeed mu- 
ricids are considered a particularly serious menace to epi- 
faunal bivalves (GALTSOFF, 1964). Boring is effected by a 
largely chemical means by way of a cocktail of acids, en- 
zymes, and chelators delivered by the accessory boring 
organ (ABO) located in the foot and is assisted by the 
rasping action of the radula (reviewed by CARRIKER, 1981). 
What effect does the thick mytilacean periostracum have 
on the actions of these boring gastropods? 


EXPERIMENTAL INVESTIGATION 


Simple choice experiments were designed to test the rel- 
ative susceptibility of mussels with and without a thick 
periostracum to boring muricid attack. Predators were of- 
fered the choice of prey with one valve possessing an intact 
periostracum and the other from which the periostracum 
had been removed. Dogwhelks are known to display marked 
preferences for borehole site and that this preference is 
learned, such that an individual may show gradual im- 
provement in accuracy of borehole siting with experience 
(HUGHES & DUNKIN, 1984). In view of this it was con- 
sidered inappropriate to test the hypothesis by using shaved 
regions of the same valve. By using whole valves to rep- 
resent the choices it was hoped to nullify the effects of 
individual preferences for boring various parts of the valve, 
lest these preferences overrode the presence or absence of 
the periostracum. These experiments were carried out by 
E.M.H. at Dunstaffnage Marine Laboratory, Oban (Scot- 
land) during May and October 1991 and the Swire Marine 
Laboratory, Hong Kong during July 1991. 


Scottish Experiments 


Small individuals of Mytilus edulis (Linnaeus, 1758), 7- 
20 mm, were collected from the intertidal zone of Dun- 
staffnage Bay, Oban (grid reference NM 886340). Poten- 
tial prey were selected which were free from marginal 
damage and adherent epibionts, and which also appeared 
to possess a complete periostracal cover. One valve of each 
individual, either left or right, was then shaved with a 
scalpel blade to remove all the periostracal sheet, thus 
exposing the calcareous shell below. Individuals of Nucella 
lapillus were collected from the small bay east of Camas 
Rubha na Liathaig, close to Dunstaffnage Bay (grid ref- 
erence NM 878344), where they were observed feeding 
on both mussels and barnacles. No size selection of the 
predators was made. Five experiments were run in outdoor 
tanks supplied with flowing natural seawater, running to 
waste. The water temperature ranged between 12°C and 
13°C. Approximately 100 mussels were used in each tank 
and the relative proportion of left and right shaved valves 
was noted (see Results). Individuals were randomly scat- 
tered and allowed to attach singly on both the floor and 
sides of the tank. Formation of aggregates was discouraged. 


Page 37 


Two days elapsed before introduction of the predators. 
This delay had two purposes; firstly, to allow the mussels 
to adopt their natural orthothetic position (with commis- 
sure perpendicular to the substratum), thus exposing both 
valves equally to the predators and secondly, to allow the 
newly exposed shell surfaces to acquire an adsorbed coating 
of metabolic products from the mussels. CARRIKER & VAN 
ZANDT (1972) discovered that the muricid Urosalpinx ci- 
nerea (Say) was attracted to the shells of the oyster Cras- 
sostrea virginica Gmelin, 1789, by material adsorbed onto 
the exterior of the shell. It was, therefore, important that 
the action of shaving the valves did not remove these cues, 
making the shaved valve less attractive. Although we do 
not know whether two days is sufficient to acquire a rea- 
sonable “biofilm” it is likely that there would be some 
reparation within this time. After this rest period, 30-40 
dogwhelks were introduced to each tank. 

Frequent observations were made on the feeding be- 
havior of the muricids and the defensive behavior of the 
mussels. All eaten bivalves were retrieved and the following 
information recorded: valve height, method of attack, 
whether the attack was on the left or right valve, the 
position of any boreholes, and whether they passed through 
the periostracum or not. The same information was re- 
corded for any failed boreholes on these and the surviving 
mussels. Each trial lasted 15-20 days. 


Hong Kong Experiments 


In Hong Kong a single experiment was run with the 
methods and experimental set up being essentially as above. 
Small individuals (up to 30 mm) of the green lipped mussel 
Perna viridis were obtained from the intertidal zone at Wu 
Kwai Sha (New Territories). Predatory Morula musiva 
(Kiener, 1835) were collected on the shore at Cape d’Agui- 
lar (Hong Kong Island). Morula musiva appears to be an 
experienced predator of mussels, having been observed 
boring Perna and Brachidontes variabilis (Krauss, 1848) on 
the shores at Wu Kwai Sha, while members of the Cape 
d’Aguilar population bored Septifer virgatus and Hormo- 
mya mutabilis (Gould, 1861) in aquaria. Seawater tem- 
peratures during the investigation fluctuated between 30°C 
and 32°C. 


Survey of Periostracal ‘Thickness 


Many of the mussels available at the chosen localities 
had incomplete periostraca. In order to survey the changes 
in periostracal thickness across the valve, 10 individuals 
of 20 mm Mytilus edulis, with apparently intact periostraca, 
were collected from Dunstaffnage Bay (Oban). Sections 
along the maximum growth direction were made from the 
valves which had been set into resin blocks to prevent the 
periostracum spalling off during sawing. Cut surfaces were 
then polished and etched slightly. Traverses were made 
along the section using scanning electron microscopy and 


Page 38 


The Veliger, Vol. 36, No. 1 


Table 1 


Experimental results of choice trials involving muricids 
and mytilids. The null hypothesis used states that there is 
no preference between boring valves with or without a 
periostracal covering. Analysis by x? one-sample test: — 
= P > 01055 = P< 0105 a) Pe OO eee 


0.001. 
Number Number 
in shaved in intact 
Total valves valves 
Predator number (left, (left, 
and prey bored right) right) PR 
Nucella lapillus 1 55 40 15 ie 
vs. Mytilus edults (15325) (7, 8) 
& 2 26 18 8 — 
(5, 13) (4, 4) 
ie 3 32 26 6 ee 
(135, 13) (2, 4) 
uf 4 55 43 12 ence 
(15, 28) (8, 4) 
sf 5 27 22 5 a 
(11) (52) 
Morula musiva 26 19 7 be 


vs. Perna viridis (9, 100) (1, 6) 


changes in thickness of both periostracum and shell re- 
corded. 


RESULTS anpD ANALYSIS 


Both Mytilus edulis and Perna viridis were readily preyed 
upon by the muricid gastropods. The vast majority of 
recorded attacks were boreholes through a single valve, 
although a small number (11%) of Mytilus were edge- 
bored, damaging both valves. These edge-bored victims 
were excluded from the statistical analysis, as were the 
small number of Perna which were taken with no apparent 
valve damage. Table 1 records the relative number of suc- 
cessful boreholes through both intact and shaved valves. 
In all experiments the number of complete boreholes sus- 
tained by the shaved valves exceeded that of those with a 
continuous periostracal cover. 

The positions of completed borings in Perna and in one 
of the Mytilus experiments are shown in Figure 1. Al- 
though boreholes were recorded from most regions of the 
valves it is clear that the majority are located in the pos- 
teriodorsal position, although many are also sited close 
against the valve margins. 

Recognizable failed boreholes were infrequent (Mytilus, 
n = 8, and Perna, n = 4). This is presumably because of 
the artificial conditions employed here and also because of 
the problems of identifying boreholes abandoned during 
the very earliest stages. Active defense by the prey was 
observed including valve flapping and flailing of the foot 

observed by WAYNE (1987), while intraspecific aggres- 

ion was displayed by individuals of Nucella lapillus along 


Figure 1 


Positions of boreholes. A. Mytilus edulis bored by Nucella lapillus 
(experiment 4) in Table 1. B. Perna viridis bored by Morula 
musiva. Closed circles indicate bores made in the shaved valves 
and open circles those in unshaved valves. 


with interloping behavior as described by HUGHES & 
DUNKIN (1984). 


Analysis 


Since the epibyssate mytilids are equivalve, the areas of 
both the shaved and intact valves are equal, and since they 
adopt an orthothetic life position, both valves are equally 
exposed to predation. Although SEED (1969) has proposed 
that dextrally coiled muricids are likely to prefer to bore 
the right valves of mussel prey there has been no statistical 
evidence to verify this for smaller mussels (e.g., WICKENS 
& GRIFFITHS, 1985; BUYANOVSKY, 1992), although Buy- 
anovsky does suggest that there is a preference for the right 
valve in mussels in the size class 20-34.9 mm. Analysis of 


E. M. Harper & P. W. Skelton, 1993 


Table 2 


Data showing the original ratio of mussels with shaved 
left and right valves and the ratio in which these were 
bored. The null hypothesis used states that there was no 
preference for boring right or left valves. Analysis by x? 
one-sample test fails to reject this null hypothesis. 


Ratio of 
Original attacks 
ratio of on left 
left and = and 
right right 
shaved — shaved 
Predator and prey valves valves x? 


Nucella lapillus vs. Mytilus edulis 63:59 22:3 3298 


34:76 917 0.17 
43:75 US 57/ 1B5 
61:94 23:32 =0.14 
40:53 14:13 0.87 
Morula musiva vs. Perna viridis 43:68 10:16 0.001 


the data from these experiments (Table 2), using a x? one- 
sample test fails to reject the null hypothesis (at the 5% 
level) that shaved right and left valves are bored in the 
same proportions as their relative abundance in the tank 
(z.e., their encounter rate). Therefore, if the presence or 
absence of periostracum is of no consequence to the actions 
of a boring muricid we might expect boreholes to be equally 
distributed between the shaved and intact valves (the null 
hypothesis). Table 1 shows that in each experiment most 
boreholes were located on the shaved valve. Analysis by a 
x? one-sample test rejects the null hypothesis for five out 
of the six trials at the 5% level of significance. In only one 
of the experiments, that with the smallest data set (n = 
26), is there a failure to reject the null hypothesis at the 


Table 3 


Periostracal thickness recorded at key points on the shell 
of each of 10 individuals of Mytilus edulis collected from 
Dunstaffnage Bay, Oban (Scotland). 


Thickness in 


digestive gland Thickness at valve 


Individual region (um) margin (um) 
1 65 70 
2 11 30 
3 9 DBs 
4 Nil 20 
5 8 20 
6 21 Ia 
7 8 Ne 
8 4 1 /s 
Y) 10 19* 

10 0) 12s 


* Denotes areas at the valve margin where the periostracum 
is already eroded, exposing the central vacuous layer. 


Page 39 


5% level. Further analysis using a 2 X 2 contingency table 
(right and left valves versus shaved and unshaved valves) 
for each of the data sets prove non-significant (P > 0.05) 
for any side on the preference for shaved and unshaved 
valves. There is, therefore, a statistically significant pref- 
erence for boring the valve without a periostracum. It is 
interesting to note that in the small number of cases where 
the valve margins of both valves were bored the hole was 
asymmetric, being more developed on the shaved valve. 
This situation did not necessarily correspond with the mur- 
icids sitting on that side of the shell. 

The distribution of periostracum over the entire valve 
surface of Mytilus edulis was recorded for 10 individuals 
in which the layer was apparently intact. Table 3 shows 
the recorded thicknesses at two key points for each of the 
studied individuals; the valve margins and the area above 
the digestive gland. There is a considerable amount of 
variation in initial periostracal thickness among individ- 
uals, as measured where it lips over the valve edge. Values 
ranged between 20 and 70 um, and similar variation has 
been observed in mussels from other localities. The cause 
and possible adaptive significance of this variation is as 
yet unclear. The periostracum of Mytilus edulis is char- 
acterized by its tripartite structure with a vacuous central 
layer being flanked by apparently solid layers (DUNACHIE, 
1963). This well-defined structure allows easy recognition 
of incomplete periostracum; well worn areas frequently 
show that the outer and middle layers are missing, or 
partially complete. Not surprisingly, in each of the tra- 
verses periostracal thickness diminished towards the umbo 
region, although the decline was not necessarily gradual 
and progressive. In some cases distinct patches were thinned 
surrounded by more pristine areas. Eight of the 10 indi- 
viduals possessed less than 10 wm cover on the older parts 
of the shell. 


DISCUSSION 


Drilling muricids are capable of penetrating mussel peri- 
ostracum (see also CARRIKER, 1978), but there is a definite 
preference for boring mussels without the layer. There are 
two possible implications of this apparent preference; e1- 
ther the presence of the periostracum in some way inhibits 
the boring action, or the denuded surface is favored as a 
resting site for the gastropod while boring. Of these two 
options we favor the former. Although it has been suggested 
that some muricids do show positive thigmotaxis there is 
no evidence here that these gastropods were showing this 
preference. The shaved valves were in many cases actually 
smoother than the those with periostracal cover, in par- 
ticular those which had become worn so as to expose the 
central vacuous layer of the sheet. 

How then does the presence of a thick periostracum 
inhibit boring? Removal of the periostracal layer is not 
likely to make the bivalve more vulnerable because of the 
overall decrease in valve thickness: not only is this decrease 
negligible (for a 20 mm Mytilus removal of the periostra- 


Page 40 


The Veliger, Vol. 36, No. 1 


cum only reduces the thickness of the most frequently 
attacked part of the shell by perhaps only 1-2%) but also 
there is no evidence that gastropods have any mechanism 
for gauging prey shell thickness (KABAT, 1990). 

GABRIEL (1981) tested the susceptibility of various shell 
microstructures to destruction by abrasion and acidic and 
enzymic attack, in mimicry of gastropod boring. Unfor- 
tunately she did not test the ability of the periostracum to 
resist components of the ABO secretion. The periostracum 
contains a sclerotized tanned protein which is chemically 
fairly inert and durable (SALEUDDIN & PETIT, 1983). These 
features may make the sheet less vulnerable to the ABO 
secretions than other organic material in the shell. The 
structure of the intact periostracum is very dense and this 
may impede penetration by ABO secretions; indeed CarR- 
RIKER (1978) notes that the chemical dissolution of the 
periostracum is accelerated on damaged areas. Addition- 
ally, the tanned nature of the periostracum imparts a de- 
gree of hardness which may impede action of the radula. 
TAYLOR & LAYMAN (1972) measured the physical prop- 
erties of most bivalve shell microstructures, including mi- 
crohardness. However, they restricted their survey to cal- 
careous parts of the shell and therefore did not tackle the 
periostracum. Preliminary studies suggest that the brittle- 
ness of the mussel periostracum does not readily lend itself 
to determining accurately microhardness. 

Additionally, in Mytilus edulis the three-layered struc- 
ture of the periostracum, with its central vacuolated layer, 
may inhibit the boring action by yielding under radular 
pressure, so preventing the radula teeth from penetrating 
the dense outer layer (acting in a manner similar to foam 
packing). However, this hypothesis remains to be tested. 

TAYLOR (1990) demonstrates that Morula musiva and 
Thais clavigera Kuster, 1858, are frequently thwarted in 
their attempts to bore the mangrove oyster Saccostrea cu- 
cullata (Born, 1778) by the conchiolin layers within the 
prey shell. Failed boreholes frequently terminate at these 
layers and those borings which do penetrate them are often 
of reduced diameter at that point. In the field he discovered 
that most actively boring muricids were in the act of pen- 
etrating the conchiolin when disturbed. The implication 
of these observations are that the conchiolin sheets, which 
are of similar composition to molluscan periostracum, are 
more difficult to bore through than the foliated calcite. 
This additional protection is particularly valuable in these 
oysters as their shell structures have been shown by Ga- 
BRIEL (1981) to be the most susceptible of all molluscan 
shell structures. Various other authors, for example LEwy 
& SAMTLEBEN (1978), have suggested that members of the 
infaunal genus Corbula derives similar benefit in defence 
against naticid gastropods from its intra-shell conchiolin 
sheets. 

We have no evidence that boreholes started in valves 
with periostracum are often abandoned; indeed as noted 
the number of failed boreholes was small (however, it 
should be noted that boreholes may be abandoned at a 
stage before they are readily perceived). It would, there- 


fore, seem that the presence of periostracum deters com- 
mencement of boring rather than decreasing the likelihood 
of success once started. Both Nucella and Morula spend 
long periods of time inspecting potential prey items before 
boring; HUGHES & DUNKIN (1984) estimate 1-2 hours for 
the former. The implication is that the muricids are ca- 
pable of selecting areas of absent or thin periostracum 
before feeding begins. It is now well known that dogwhelks 
feed optimally (BURROWS & HUGHES, 1990; HUGHES & 
Burrows, 1990) and are capable of making economic “de- 
cisions” balancing energy gain from a particular prey choice 
against energy and time expended in obtaining it. 

Boring is a time consuming process, each meal taking 
several days to complete. In the natural environment fail- 
ure to complete a borehole may result from adverse en- 
vironmental conditions, for example desiccation during low 
tide, attack by a predator, or displacement by a competitor. 
In these experiments the participants were not exposed to 
a tide or other predators. It should also be noted that several 
of the failed boreholes occurred on specimens with com- 
pleted holes and that in these instances two gastropods 
were observed simultaneously boring the same prey item. 
In this case failure to complete the bore results from one 
gastropod reaching the flesh before the other, rather than 
any other reason. 

Many studies have revealed a pronounced stereotypy in 
borehole positioning and the distribution recorded here 
parallels that noted by HuGHEs & DUNKIN (1984) for 
Nucella boring in Mytilus both in the laboratory and the 
field, and TONG (1987) for Morula boring Brachidontes 
variabilis. Our laboratory observations show that Morula 
also utilized the same position when boring other mytilids 
Septifer virgatus and Hormomya mutabilis. A number of 
different hypotheses have been advanced to explain this 
preference for the older parts of the shell. GRIFFITHS (1981) 
postulates that the narrower part of the mytilid shell may 
be easier to grip, but this explanation is probably only 
reasonable in a consideration of naticid predation rather 
than for muricids which do not hold the prey in the foot 
while boring. HUGHES & DUNKIN (1984) suggest that this 
position gives rapid access to the digestive gland, the most 
calorifically rewarding part of the flesh, and that the more 
experienced the dogwhelk, the more accurately the bore- 
hole is located. In these experiments we found that often 
the muricids failed to consume the entire prey, leaving 
residual mantle and foot tissue behind, again implying that 
consumption of the the digestive gland and other viscera 
is favored. HUGHES & DUNKIN (1984) also made the puz- 
zling assertion that this preferred boring site also corre- 
sponds to the thinner parts of the shell. Evidence from the 
traverse study shows a gradual thickening of the shell away 
from the valve edge. This is in accordance with the bivalve 
mode of growth whereby shell material is continuously 
added by the entire surface of the outer mantle fold. One 
would anticipate that the pronounced tendency to bore 
through the older parts of the shell would seem to penetrate 
the thicker shell, except in very high energy environments 


E. M. Harper & P. W. Skelton, 1993 


where the shell may be very badly abraded. However, 
periostracum is subject to thickness diminution by the 
agencies of fungal and bacterial decay, rasping of grazing 
animals, and abiotic erosion. In many bivalves, particularly 
those with thinner periostraca, the extent of the periostra- 
cal layer is restricted to the more newly formed parts of 
the shell. Indeed even in many mytilids examined the peri- 
ostracum is absent over much of the older part of the shell, 
and this study shows that even those individuals with ap- 
parently intact periostraca show substantial thinning over 
that area. It might be argued that by boring over the 
posteriodorsal region of the shell the gastropods are not 
only gaining from direct access to the more lucrative di- 
gestive gland but also from the advantage of boring in an 
area with little or no periostracal cover. 

ANSELL (1969) describes bivalve defenses as either active 
or passive. Deterrence of boring predation by the posses- 
sion of a thick periostracum falls into the latter category. 
Undoubtedly the mussels also gain defense against these 
and other predators by their tendency to clump (OKUMARA, 
1986; Lin, 1991) and also by the more active mechanisms 
described by WAYNE (1987) and PETRAITIS (1987). Peri- 
ostracum is a non-renewable defense and its value will 
wane with increased wear, but by the time it has completely 
worn away the mussels are likely to have reached a size 
refuge from their boring predators. This is especially true 
for the rapidly growing Perna viridis (SEED, 1990). 

It is tempting to speculate that other epifaunal bivalves 
with thick periostraca (e.g., members of the Arcacea) derive 
a similar benefit against boring muricids and that those 
infaunal bivalves also possessing this feature may be like- 
wise defended from attack by naticid gastropods. CLARK 
(1976) suggests that the extreme thickness of the mytila- 
cean periostracum is likely to be a derived feature. It would 
be interesting to determine whether this character resulted 
from selection pressure exerted by boring predators or 
whether thickening preceded their evolution and that the 
defensive value was merely fortuitous. The first boreholes 
attributable to the muricids occur in rocks of Lower Cre- 
taceous (Albian) age (TAYLOR et al., 1983). As yet we have 
very little evidence of fossil periostracum; the layer seldom 
survives the life time of the mollusk let alone taphonomic 
processes. However, HUDSON (1968) does recognize a 
structure on the outer surface of the Jurassic mytilid Prae- 
mytilus strathairdensis (Anderson & Cox, 1948) which he 
interprets as periostracum. Hudson measured this putative 
periostracum as having a maximum thickness of 15 wm. 
Such a value, although thicker than that recorded for many 
bivalves (Harper, unpublished), is rather lower than has 
been recorded for Recent epibyssate Mytilacea. At present 
we can only speculate on the significance of this datum. 
One possibility is that a slight relative thickening of the 
periostracum in earlier mussels may have been associated 
with their tolerance to hyposaline waters analogous to the 
condition found in many freshwater taxa (TEVESZ & CAR- 
TER, 1980); Hudson interprets the beds in which Prae- 
mytilus is found as having been deposited in brackish la- 


Page 41 


goons. If confirmed in other pre-Cretaceous mytilids 
periostracal thickening would thus have been preadaptive 
for inhibition of boring by muricids, although this addi- 
tional selection presure may well have led to yet further 
thickening thereafter. Yet we have no way of telling wheth- 
er these specimens of Praemytilus possessed fully intact 
periostraca nor any comparative data for other Jurassic 
mytilids. Further evidence from palaeontological material 
is required to resolve the question of the primary cause 
for thickening of the periostracum in these bivalves. 


ACKNOWLEDGMENTS 


This research was funded by NERC. The Directors of 
the Dunstaffnage Marine Laboratory and the Swire Ma- 
rine Laboratory (University of Hong Kong) are gratefully 
acknowledged for their permission to use their facilities. 
Mike Burrows provided useful discussion on dogwhelk 
foraging. Comments by A. R. Palmer were very valuable 
and have improved this paper. 


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THE VELIGER 


: © CMS, Inc., 1993 
The Veliger 36(1):43-68 (January 4, 1993) 


Morphological and Allozyme Variation in 
Littorina sitkana and Related Littorina 
Species from the Northeastern Pacific 

by 


ELIZABETH GRACE BOULDING! 


Department of Zoology NJ-15, University of Washington, Seattle, Washington 98195, USA 


JOHN BUCKLAND-NICKS? 


Department of Zoology, University of Alberta, Edmonton, Alberta T6G 1E9, Canada 
AND 


KATHERINE LYN VAN ALSTYNE? 


Department of Zoology NJ-15, University of Washington, Seattle, Washington 98195, USA 


Abstract. We studied the morphological and biochemical systematics of some Littorina with direct 
development from the northeastern Pacific. We describe differences in geographic distribution, body 
pigmentation, size at first reproduction, shell morphology, and behavior between L. sp. and its close 
relative L. ‘“‘kurila.”. We also discuss field characters useful in distinguishing L. sp. from L. sitkana 
Philippi, as these two species often have an overlapping distribution on northeastern Pacific shores of 
intermediate exposure. The systematics of these gastropods are difficult because there is considerable 
within-species variation in shell morphology. There was more variation in shell shape within split 
broods of L. sp. grown at high and low growth rates than was seen among three different taxa collected 
in the field. Even shell ornamentation was not always diagnostic; offspring of heavily ridged L. sitkana 
parents were completely smooth when cultured at high growth rates. 

Littorina sitkana and L. sp. from areas of intermediate wave exposure on Tatoosh Island, Washington, 
did not hybridize. The two populations were fixed or nearly fixed for different allelic allozymes at the 
Pep-3, Gpi-1, Sdh-4, and Pgm-1 loci and had distinctive esterase banding patterns. This agrees with 
our conclusions from our morphological and hybridization studies that L. sitkana and L. sp. are separate 
species. Our electrophoresis results suggested that L. sp. was closely related to L. subrotundata (Carpenter); 
however, the two taxa had fixed differences at the Pep-3 locus. We estimated a preliminary phylogeny 
based on allozyme data for these northeastern Pacific Littorina and for L. saxatilis, L. obtusata, and L. 
littorea from the northwestern Atlantic. 


INTRODUCTION 


' Present address: Dept. of Biological Sciences, Simon Fraser Geatonnie oP Che conus Lateran Gancn Rig, 1089) tae 
Ciniveraliy, |Bummneloyjy mitisin (Colwilales Weiss US (Cece habit the intertidal zone on rocky shores over much of the 


? Present address: Dept. of Biology, St. Francis Xavier Uni- 2 
versity, Antigonish, Nova Scotia, B2G 1C0, Canada. north temperate zone. They have been the subjects of nu- 


> Present address: Dept. of Biology, Kenyon College, Gambier, merous studies contributing to intertidal ecology and pop- 
Ohio 43022, USA. ulation genetics (see reviews by RAFFAELLI, 1982; BERGER, 


Page 44 


1983; FALLER-FRITSCH & EMSON, 1985; JANSON, 1987). 
The results of such studies will be misleading if, unknown 
to the investigator, the populations being studied contain 
a mixture of species. As a result of recent systematic work 
in Britain, Littorina saxatilis (Olivi, 1792) has been split 
into three to four species and Littorina obtusata (Linnaeus, 
1758) has been split into two species (reviews by FRETTER 
& GRAHAM, 1980; JOHANNESSON & JOHANNESSON, 1990; 
RAFFAELLI, 1990; REID, 1990; WARD, 1990). 

Recent work has helped clarify the status of oviparous, 
direct-developing littorinid species from the northern Pa- 
cific (BOULDING, 1990a, b; REID, 1990; REID & GOLIKOV, 
1991; REID ef al., 1991). BOULDING (1990a) mentioned 
Littorina sp., a new subspecies of Littorina kurila Midden- 
dorff that was related to Littorina sitkana Philippi and lived 
on Tatoosh Island and other wave-exposed shores in the 
northeastern Pacific. The morphological similarity be- 
tween L. sp. from Tatoosh Island and L. kurila Midden- 
dorff from Adak Island had been initially recognized by 
Reid (D. G. Reid in lit. to E. G. Boulding). REID (1990, 
note added in proof) examined the syntypes of L. kurila 
Middendorff and found the pallial oviducts were of the 
form found in L. sztkana. He suggested that L. kurila Mid- 
dendorff was a junior synonym of L. sitkana Philippi and 
that a new name might be necessary for the species he 
referred to as L. “‘kurila.””. Reid included both specimens 
from Adak Island in the Aleutians and specimens from 
Tatoosh Island in L. “kurila.”’ In her thesis BOULDING 
(1990b) considered the Tatoosh Island form to be a taxon 
separate from the Adak Island form. She discussed the 
morphological and allozyme characters distinguishing these 
two taxa from each other and from L. sitkana. REID & 
GOLIKOV (1991) have suggested that L. sp. and L. “kurila” 
(sensu BOULDING, 1990b) be included in the taxon L. sub- 
rotundata (Carpenter, 1864) because they found no dif- 
ferences in the pallial oviducts of these three taxa. 

The above illustrates that the systematics of Littorina 
are difficult, especially if based only on shell morphology, 
because the degree of morphological variation within spe- 
cies is large relative to the variation between species. In 
general, measurement of gastropod shells is challenging 
because there are few homologous points (BOOKSTEIN et 
al., 1985; A. J. Kohn, personal communication). The pa- 
rameters used by Raup to model shell shape (RAupP, 1961, 
1966) are difficult to measure on an intact shell (KOHN & 
RicGs, 1975; Schindel, unpublished manuscript). Never- 
theless, it is worthwhile to attempt to separate species with 
similar morphology on the basis of their shell characters 
because such characters can be measured on recovered 
shells, on museum specimens, and on fossils, and because 
they were used exclusively in the early species descriptions 
of these littorinids (PHILIPPI, 1846; MIDDENDORFF, 1848; 
CARPENTER, 1864; DALL, 1921; OLDROYD, 1927; PALMER, 
1958). Previous workers working on closely related species 
of Lillorina have used discriminant analysis and principal 
component analysis to look for morphological separation 
of different groups (MURRAY, 1982; WELLINGTON & KurIS, 


The Veliger, Vol. 36, No. 1 


1983; JANSON & SUNDBERG, 1983; JANSON, 1985; JANSON 
& WarD, 1985). With these methods the information in 
a number of morphometric variables can often be reduced 
to two or three composite variables that summarize most 
of the information and differentiate between the groups 
better than any two or three morphometric variables could 
do alone (REYMENT et al., 1984). 

That shell morphology of gastropods varies with envi- 
ronmental conditions has long been known (COLTON, 1922; 
CROTHERS, 1971; VERMEIJ, 1980). The shell shape of 
Littorina littorea Linnaeus, 1758, has been shown to change 
dramatically with growth rate (KEMP & BERTNESS, 1984). 
Shell morphology has been shown to change with prox- 
imity to crabs preying on conspecific gastropods (AP- 
PLETON & PALMER, 1988; PALMER, 1990). This plasticity 
in shell form leads to problems of species determination 
when snails from different locations are compared because 
the observed morphological differences might have a ge- 
netic component or they might be caused solely by envi- 
ronmental differences among the different locations. To 
investigate the genetic basis of morphological differences 
in shell morphology we raised the offspring of parents 
collected from various field sites in a “common garden” 
and compared the morphology of these offspring; this pro- 
cedure is rare in the zoological literature. 

Another method of distinguishing morphologically sim- 
ilar species is protein electrophoresis. Electrophoresis has 
been frequently used to separate morphologically similar 
but reproductively isolated species complexes; if two sym- 
patric taxa are shown to be fixed for different alleles at a 
locus of the same allozyme, the two taxa must be repro- 
ductively isolated (FERGUSON, 1980; BUTH, 1984). 

Allozyme electrophoresis has been used to clarify the 
status of sibling species pairs such as Littorina saxatilis 
(Olivi) and Littorina arcana Hannaford Ellis, 1978 (WARD 
& WARWICK, 1980; WARD & JANSON, 1985; KNIGHT & 
WarD, 1991). The latter two species are particularly in- 
teresting because their shell morphology is almost identical 
(HANNAFORD ELLIS, 1979) and there are no known unique 
allelic allozymes that can be used to distinguish them (WARD 
& WARWICK, 1980; WARD & JANSON, 1985); however, 
the juveniles of the first species emerge from the brood 
pouches of their mothers, whereas the juveniles of the 
second emerge from benthic egg masses (HANNAFORD EL- 
Lis, 1979). Recently MAsTRO et al. (1982) used electro- 
phoretic data to verify the status of the L. scutulata species 
complex, which has been previously separated into two 
species on the basis of penis shape and egg capsule mor- 
phology (MurRRAY, 1979, 1982). 

Another major contribution of allozyme electrophoresis 
to systematics is in the construction of phylogenies of closely 
related species (FERGUSON, 1980; BUTH, 1984). Electro- 
phoretic data can be used to construct a phenetic or a 
phylogenetic classification using genetic distance data or 
using alleles as characters (WILEY, 1981; BUTH, 1984). A 
recent major advance in the construction of such phylog- 
enies is the ability to put confidence limits on different 


E. G. Boulding et al., 1993 


branches of the phylogeny by bootstrap methods (see FEL- 
SENSTEIN, 1985). This is necessary because usually several, 
and often many, cladograms with a similar degree of par- 
simony can be constructed from one character matrix (FEL- 
SENSTEIN, 1982, 1985). 

In this paper we compare the morphology of Littorina 
sitkana Philippi, 1846, with that of L. “kurila” (REID, 
1990) and with that of a wave-exposed shore taxon Lit- 
torina sp. All three taxa lay benthic egg masses which 
develop directly into juvenile snails (see BUCKLAND-NICKS 
et al. [1973] for L. sitkana; this paper for the other two 
taxa). These three taxa have very similar shell morphology 
and external anatomy and some gastropod systematists 
have lumped them together. Kohn examined the shell mor- 
phology and external anatomy of L. sitkana and L. sp. from 
Tatoosh Island, the major locality studied here, and con- 
cluded that both were the same species (A. J. Kohn, per- 
sonal communication). 

We used allozyme electrophoresis to distinguish Litto- 
rina sitkana and L. sp. on Tatoosh Island, Washington. 
The results of this enabled us to find more subtle mor- 
phological characters that make it possible to identify them 
in the field. We also had some success distinguishing the 
three taxa on the basis of shell shape alone; we used dis- 
criminant analysis of shell shape to classify adult L. sp., 
L. “kurila,” and L. sitkana collected in the field and found 
that individual snails were assigned to the correct taxon 
90% of the time. However, even multivariate analysis of 
shell shape can be misleading; when broods of L. sp. were 
split and cultured in the lab at two densities—but under 
otherwise identical conditions—the observed differences in 
shell shape were greater between the two densities than 
among field-collected snails of the three taxa. We also 
report the results of breeding experiments in which at- 
tempts were made to hybridize various populations of L. 
sitkana, L. sp., and L. “kurila.” On the basis of reproductive 
characters, attempts at hybridization, and electrophoretic 
data from ten allozymes, we conclude that L. sitkana is 
distinct from L. sp. and also from L. “kurila.” Our allozyme 
evidence showed that L. sp. and L. sitkana were fixed for 
different alleles at three loci on Tatoosh Island, Wash- 
ington. We show that L. subrotundata was closely related 
to L. sp. but was fixed for different alleles at the Pep-3 
locus. Littorina sp. was closely related to L. “kurila” but 
was more distantly related to L. sztkana. We construct a 
preliminary phylogeny based on allozyme data for these 
and other taxa of Littorina from locations along the north- 
eastern Pacific and from Rhode Island in the northwestern 
Atlantic. We show that none of these North Atlantic species 
is conspecific with L. sp. or L. sitkana. 


MATERIALS anD METHODS 


Collection and Identification of Snails for 
Morphometry 


Littorina sitkana was collected at ten sites from Siletz 
Bay, Oregon, north to Massacre Bay, Attu Island, Alaska 


Page 45 


(Table 1). Littorina sp. was collected from six sites span- 
ning from Whale Cove, Oregon north to near Sitka, Alaska 
(Table 1). More than 100 L. “‘kurila”’ were collected from 
Sweeper’s Cove, Adak Island, Alaska (Table 1) at the same 
location and on the same field trip (VERMEIJ et al., 1990) 
as some of the specimens used by D. G. Reid (REID, 1990); 
they were identical in size, shell coloration, and shape to 
specimen “‘m” in Reid’s photograph labelled L. kurila (REID, 
1990:4) and relabelled L. “‘kurila” in a note added in proof 
of REID (1990). We use L. “‘kurila” to refer to the Adak 
animals in what follows to avoid using L. sp1 and L. sp2. 

After collection, adult snails were held in free-flowing 
seawater in outdoor tanks at Friday Harbor Laboratories, 
Washington (Table 1). Openings were cut in 10 cm x 10 
cm X 4 cm high polyethylene sandwich containers or 93- 
mm diameter petri dishes over which 1.1-mm nylon mesh 
was fastened with hot melt glue. This allowed water flow 
but did not permit the snails to escape. 


Multivariate Analysis of Morphological 
Changes with Growth Rate 


To see how shell morphology changed with growth 
rate, we used discriminant analysis to compare the mor- 
phology of cultured snails with that of snails collected 
in the field. The snails in our “field” collected treatments 
and the parents of snails in our experimental treatments 
were collected from the field: Littorina sp. was collected 
from the Finger on Tatoosh Island, L. sitkana was col- 
lected from North Island Draw on Tatoosh Island dur- 
ing 15-16 September 1989, and L. “kurila” was col- 
lected from Sweepers Cove on Adak (Table 1). 

For our experimental treatments we cultured juve- 
niles at various densities in dishes in outdoor tanks. The 
dishes were made by drilling 35-mm holes into the top 
and bottom halves of 93-mm diameter petri dishes. We 
used Optilux® petri dishes made by Falcon. These are 
made of clear styrene plastic, which lets most of the 
sunlight through and encourages algal growth inside 
the dishes. Nitex® mesh (243 wm) was glued inside the 
holes in the top and bottom of the dish. A styrofoam 
float was glued to the outside of the top of the dish with 
hot melt glue. A pebble was placed inside each dish as 
ballast. The two halves of the petri dishes were held 
together by elastic bands. When the dish was placed in 
the water it filled and floated on edge, an orientation 
that allowed maximum water flow through the dish. 

The dishes quickly became coated inside and outside 
with diatoms. The outside of each dish was cleaned 
periodically with a plastic scrub brush to allow in more 
light. This increased the biomass of diatoms growing 
on the inside of the dish where they were available to 
the snails. Dishes with a high density of snails were 
rasped clean on the inside of the dish; dishes with a 
lower density of snails had a visible coating of diatoms 
on the inside. 


Page 46 


The Veliger, Vol. 36, No. 1 


Table 1 


Location of collection sites for electrophoresis. 


Site 


Massacre Bay, Attu Is., Alaska 
Sweeper Cove, Kuluk Bay, Adak Is., Alaska 


Hoonah, Alaska 
Whitestone Harbor, Alaska 
Bamfield, B.C. 

Tatoosh Is., Washington 


Shi Shi, Washington 
Waatch River, Mukkaw Bay, Washington 


Grays Harbor, Washington 

Siletz Bay, Oregon 

Bass Rock Road, Rhode Island 
(South of Narragansett Pier) 


Friday Harbor, Washington 


We had two experimental treatments of Littorina sp. 
from Tatoosh: sparse and dense. ‘The parents were col- 
lected from the field as juveniles (shell length 1.5—2.5 
mm) and were isolated in unsexed pairs in culture dishes 
with 243-um Nitex® mesh over the openings. ‘The sex 
ratio of the parents was not significantly different from 
50:50 and 22 out of 23 of the pairs with one female 
and one male produced egg masses which hatched be- 
tween October 1987 and June 1988. The eggs remained 
in the parents’ dishes until the largest juvenile in a dish 
had reached a shell length of about 1 mm. The juveniles 
were then split into two initial densities: sparse (10 
juveniles per dish) and dense (30 juveniles per dish). 
To split the broods, the largest 40 juveniles were first 
divided into two groups of 20 by starting with the largest 
juvenile and placing it in the first group, then putting 
the second largest in the second group, then the third 
largest in the first group, and so on. Then the first group 
was split into two groups of 10 using the same proce- 
dure. The dense dish contained the other group of 10 
plus the group of 20. A random number table was used 
to decide whether the largest juvenile was put in the 
first or second group but the rest of the procedure was 
done systematically. Some mortality occurred soon after 
this procedure so that the density of the sparse treat- 
ments at the time of measuring ranged from 2 to 9 with 
a mean of 6 (SD 2.3, n = 15); the density of the dense 
treatments ranged from 6 to 15 with a mean of 12.7 
(SD 3.3, n = 15). These are referred to as the “sparse 
L. sp.” treatment and the “dense L. sp.” treatment 
respectively. Other L. sp. were raised loose in a large 
plexiglass tank about 1 m x 2 m X 0.5 m deep. 

We had one experimental treatment of Littorina “‘ku- 
rila,” the dish L. “‘kurila” treatment. Littorina “kurila”’ 
from Adak Island were raised by removing eggs close 


Species collected 


52°50'N, 173°40'E 
51°51'N, 176°39'W 


Littorina sitkana 
Littorina sithana 
Littorina “‘kurila” 
Littorina sitkana 
Littorina sitkana 
Littorina sp. 

Littorina sitkana 
Littorina sp. 

Littorina sp. 

Littorina sitkana 
Littorina subrotundata 
Littorina subrotundata 
Littorina sitkana 
Littorina littorea 
Littorina obtusata 
Littorina saxatilis 
Lacuna sp. 


58°08'N, 135°28’W 
57°15'N, 135°34'W 
48°50'N, 125°08’W 
48°23'N, 124°44'W 


48°16'N, 124°36'W 
48°21'N, 124°40'W 


46°54'N, 124°05'W 
44°56'N, 124°01’W 
41°25'N, 71°30'W 


48°30'N, 123°85'W 


to hatching from the sandwich containers of their par- 
ents and placing them in a culture dish. The early 
juvenile stages were reared at densities from 18 to 27 
per dish with a mean of 23.7, while later juvenile stages 
were raised at densities of 1 to 14 with a mean of 7.6 
(SD 4.35, n = 18). At the time of measuring, the den- 
sities ranged from 1 to 14 with a mean of 6.35 (SD 4.0, 
n = 30). 

We had one experimental treatment of Littorina sit- 
kana, the “‘tank L. sitkana”’ treatment. Littorina sitkana 
from ‘Tatoosh Island were raised in culture dishes at 
densities from 1 to 10 adults per dish and also loose in 
a large tank about 1 m X 2 m X 0.5 m deep. The 
diatom growth in this large tank was never significantly 
reduced by the grazing of snails and the maximal growth 
rates of L. sitkana exceeded those measured in the field 
(BOULDING, 1990b; Boulding & Van Alstyne, unpub- 
lished data). 

Snails from other locations (Table 1) were also held 
in petri dishes and some of these produced young; the 
shell morphology and external anatomy of these snails 
was also examined by E. G. Boulding but no multi- 
variate analysis was done. 


Shell Measurement 


Shells were videotaped under a dissecting microscope 
then digitized with an image analysis system. Preliminary 
work (BOULDING & Hay, in press) showed that most of 
the measurement error using this technique came from 
variation in the way the shell was oriented. Therefore the 
shell was consistently photographed in two orientations. 
In the “axial orientation” (Figure 2a) the shell was ori- 
ented so that a line joining the apex and base of the col- 
umella was in the plane perpendicular to the optical path 
and so that the curve of the last (body) whorl was just 


E. G. Boulding e¢ al., 1993 


hidden by the outer lip of the aperture. In the ‘“‘apertural 
orientation” (Figure 2b) the shell was oriented so that the 
outer rim of the aperture was in the plane perpendicular 
to the optical path. To reduce errors resulting from in- 
consistent orientation, an acetate grid was taped over the 
video monitor and used to ensure that the axis of coiling 
was always parallel with the horizontal grid lines of the 
monitor. 

Each snail’s video-frame number, dish number, grade 
of spiral sculpture, shell color classification, and wet weight 
were entered in a database at the time of videotaping. Shell 
sculpture was graded as 0 to 3, 0 being completely smooth 
and 3 being deeply ridged. The grades were not equivalent 
for Littorina sitkana and L. sp. since the most developed 
spiral sculpture ever seen for L. sp. did not reach that of 
L. sitkana. For this reason spiral sculpture was not included 
in the discriminant analysis. 

The measurements shown in Figure 2 (standard error 
for repeated measurements of shell length was 0.01 mm; 
BOULDING & Hay, in press) were chosen because they 
could be taken nondestructively on a living snail with a 
high degree of repeatability and because they are com- 
parable to those taken with calipers on larger snails by 
previous investigators. We measured diameters instead of 
radii as recommended by Schindel (unpublished manu- 
script). A Pascal program was written to locate the axis 
of coiling and to calculate the desired measurements from 
the digitized points. The axis of coiling was estimated by 
bisecting the angle formed by the three points marked with 
dots in Figure 2a. Shell length (SL) was defined as the 
maximum distance between the apex and a line tangential 
to the base of the columella and perpendicular to the axis 
of coiling. Shell width (SW) was measured perpendicular 
to shell length and was defined as the distance between 
the line tangent to the points on the left and right outlines 
of the body whorl farthest from the axis of coiling (Figure 
2a). The whorl width at suture (WW) was defined as the 
distance between the upper and lowermost points marked 
on the suture above the last (body) whorl (Figure 2a). The 
outer margin of the aperture was digitized to measure 
aperture area (AA) (Figure 2b). The aperture length (AL) 
was the maximum distance between point of adhesion (PA; 
Schindel, unpublished manuscript) in apertural view (Fig- 
ure 2b) and a point on the other side of the outer aperture. 
Aperture width (AW) was the maximum width of the 
outer aperture perpendicular to aperture length. 


Multivariate Analysis of Shell Shape 


We used program 7M of the BM DP Statistical Software 
Package (JENNRICH & SAMPSON, 1985) to do stepwise 
discriminant analysis and canonical variate analysis on the 
variables SL, SW, WW, AL, AW, and AA. We identified 
the snails to taxon using the characters described in the 
comparative morphology section of the results; this can be 
done with 100% accuracy for animals larger than 2 mm 
and our ability to do this correctly for the sympatric species 
pair, Littorina sitkana and L. sp., has been confirmed by 


Page 47 


allozyme electrophoresis. There were seven treatments: 
tank L. sitkana, field L. sitkana, dish L. “‘kurila,” field L. 
“kurua,” sparse L. sp., dense L. sp., and field L. sp. as 
described above, and each treatment was assigned a group- 
ing variable. All variables were log-transformed before the 
analysis to stabilize variance and the “‘jacknife” option was 
used. This ensured that the classification function used to 
determine group assignment was unbiased since the snail 
being classified had not been used to construct the function. 
We ran the program 7M twice: the first time we used only 
the three field treatments and the second time we used all 
seven treatments. 


Other Measurements 


We assessed size at sexual maturity for females by mea- 
suring the shell length at which a female confined with a 
mature male began to lay eggs; the size at sexual maturity 
for males was the size at which the penial glands of a male 
were fully developed. We determined wet weight to the 
nearest 0.1 mg by blotting a live snail and placing it on 
the tray of a Sartorius balance (model 2404). We deter- 
mined foot area for Littorina sitkana and L. sp. from Ta- 
toosh by photographing the foot of a snail actively crawling 
over an inverted petri dish. We used analysis of covariance 
(ANCOVA) with the program BMDP 1V, using an es- 
timate of shell volume (SL x SW x SW)?°° as the covariate 
to test whether the mean foot area was greater for L. sp. 
than for L. sitkana. We also used ANCOVA with shell 
volume as the covariate to test whether mean wet weight 
was greater for L. sitkana than for L. sp. 


Hybridization Experiment 


Pairs of juvenile littorinids measuring 1.5-2.5 mm in 
shell length were selected at random from a large group 
and put in culture dishes. The dishes were inspected at 
intervals between 14 April and September 1988 for the 
presence of eggs. The snails were not sexed before putting 
them in the dishes so only about half the dishes contained 
one male and one female snail. During the study some 
snails died and were replaced with another small juvenile 
snail measuring 1.5-2.5 mm. Only a few of these unsexed 
crosses involved Littorina sitkana as this first hybridization 
experiment was done for another purpose (BOULDING & 
Hay, in press). 

A second hybridization experiment was done to see 
whether different populations of Littorina sitkana were ca- 
pable of crossing with each other (Table 6). This second 
experiment also included some crosses between L. sp. and 
L. sitkana. In each dish one virgin female snail (defined as 
a female isolated from males since before it reached 2.5 
mm in shell length) and one male snail were put together. 
The dishes were put in an outdoor tank with free-flowing 
seawater in August 1988. An attempt was made to put an 
intrapopulation pair together for every interpopulation pair 
(Table 6). We tried to cross males and females from each 
site with those from other sites but for some sites no virgin 


The Veliger, Vol. 36, No. 1 


Table 2 


Enzymes screened for all species. 


Page 48 
Enzyme Enzyme Synonym 

aspartate aminotransferase Aat Got 
esterase Est 
B-N-Acetylgalatosaminidase B-Gala B-Gal 
N-Acetyl-8-glucosaminidase B-Ga B-Glu 
glucose-6-phosphate isomerase Gpi Pgi 
peptidase Pep 
phosphoglucomutase Pgm 
6-phosphogluconate dehydrogenase 6-Pgd Pgdh 
sorbitol dehydrogenase Sdh Iddh 


' Number of loci observed. 


Est a NA 


E.C. No. n! Locus Buffer Migration? 
2.6.1.1 2 Aat-1 I 0.74 
3.1.1.1 ? Est-2 I 1.15 
BE2e 153) 1 B-Gala-1 Ill 0.74 
3.2.1.30 1 B-Ga-1 Ill 0.67 
5.3.1.9 2 Gpi-1 I 0.95 
3.4.11 3 Pep-2 I 0.98 
Pep-3 I 0.58 
Dsl Sxik 3 Pgm-1 II 1.52 
1.1:1.44 1 6-Pgd Ill 0.59 
1.1.1.14 4 Sdh-4 II 0.33 
Sdh-1> Il 0.98 


? Migration of 100 allele relative to slow red dye (magenta) of red food coloring. 


> Not available for Lacuna. 


females were available. The dishes were inspected peri- 
odically for the presence of eggs until August 1989 and 
the number of dishes that produced fertile eggs was re- 
corded. We occasionally obtained infertile eggs in watery 
jelly that did not develop, but we did not count these 
because we also obtained these from virgin female-virgin 
female pairs of the same species that were left together for 
a long period. 


Collection and Identification of 
Specimens for Electrophoresis 


Littorina sitkana were collected from seven sites, L. sp. 
from three sites, L. subrotundata from two sites, and L. 
scutulata from one site along the northeastern Pacific coast. 
For comparison, L. saxatilis, L. littorea, and L. obtusata 
were collected from Rhode Island in the northwestern 
Atlantic (Table 1). Littorina “‘kurila” was collected from 
Sweeper’s Cove, Adak Island, Alaska (Table 1) at the same 
location and on the same field trip as the Adak Island 
specimens discussed by REID (1990). 

Littorina sitkana, L. “kurila,” and L. sp. were identified 
using the morphological criteria described below in the 
Results section. The L. scutulata were identified as true L. 
scululata Gould, 1849, because the females had egg cap- 
sules with unequal rims (MASTRO et al., 1982). The Lacuna 
were identified as Lacuna vincta (Montagu, 1803) using 
KOZLOFF (1987). 

David G. Reid identified the Littorina saxatilis as true 
L. saxatilis Olivi, 1792 (= L. rudis Maton 1797; FRETTER, 
1980). The L. saxatilis shells were large (shell height 9.0- 
11.0 mm), heavy, and ridged, and the females were ovo- 
viviparous. He identified the L. obtusata shells as true L. 


obtusata on the basis of their shape and relatively large 
size (shell length 8.0-10.0 mm). 
The Littorina subrotundata (= Algamorda subrotundata 


Carpenter, 1864) (= Littorina newcombiana Hemphill, 1876 


[REID, 1989]) were collected and identified by D. G. Reid. 
Note that we are using this name in its strict sense to refer 
only to the salt marsh form mentioned by REID & GOLIKOV 
(1991). 


Enzyme Assay Technique 


Snails were held in running seawater for at least a week 
and allowed to graze on benthic diatoms. Some individuals 
were stored at — 80°C until they were used and others were 
used alive. The entire body of each snail was used except 
for the embryos brooded by female Littorina saxatilis. The 
body was homogenized in an equal weight of 0.5 M Tris- 
HCI buffer of pH 7.1. The crude homogenate was ab- 
sorbed onto 12 X 2.5 mm wicks of Whatman No. 1 filter 
paper and 24-30 wicks were placed into a horizontal gel 
of 12.5% Sigma starch. Narrower wicks were dipped into 
red food coloring (FD&C Red No. 3 and Red No. 40) 
and placed between every six sample wicks. The buffer 
systems used were: (I) discontinuous, tris-citrate electrode 
buffer, pH 8.65, borate (NaOH) gel buffer, pH 8.1 (AYALA 
et al., 1973); (II) continuous, tris-borate-EDTA electrode 
and gel buffer, pH 9.1 (AYALA et al., 1973); and (III) 
amine, citric acid buffer, pH 7.0 (CLAYTON & TRETIAK, 
1972). The buffer used for each enzyme and synonyms for 
enzyme names are shown in Table 2. 

Enzyme staining procedures followed those of MASTRO 
et al. (1982) for Aat, Est a NA, Gpi, Lap, Mdh, Pgm, 
and Sdh, and those of AEBERSOLD ef al. (1987) for Est-D, 
B-Gala, B-Ga, 6-Pdg (with double the amount of NADP), 
Pep-2 (substrate glycyl-L-leucine), Pep-3 (substrate 
L-leucyl-L-tyrosine and L-leucyl-L-valine), Pgm-agar 
(with double the amount of NADP and G6PDH). Sod 
was read off the Sdh gels. Sod, Est a NA, Lap, and Mdh 
were not assayed for all species. 

When more than one locus was resolved for an enzyme, 
the fastest migrating locus is given the suffix 1, the next 
fastest 2, and so on. For each locus the most common allele 


E. G. Boulding e¢ al., 1993 


in the Tatoosh Island population of Littorina sitkana is 
labelled as 100. The average distance of migration of the 
slow red dye (magneta) was 40 mm and of the fast red 
dye (orange-red) was 120 mm. The absolute distance of 
migration of the 100 allele of each locus relative to that of 
the slow red dye is given in Table 2. An allele which was 
5 mm slower than the 100 allele on an average gel would 
be labelled 95 whereas one that was 12 mm faster would 
be labelled 112. 

Although more than one locus was resolved for most 
enzymes (Table 2), usually only one locus could be scored. 
The products of fainter loci for the same enzyme were 
often obscured by an allele of a darker locus for at least 
one species out of the nine. 

Three loci were resolved for the peptidases (Table 2). 
The substrate glycyl-L-leucine gave a faint fast band, a 
dark medium band, and a faint slow band, and the sub- 
strate L-leucyl-L-tyrosine with L-leucyl-L-leucine gave a 
faint fast band and dark medium and slow bands. 

The Est a NA stain gave at least five regions of activity 
(Figure 8a). Although esterases have been used in many 
studies of Littorina (see BERGER, 1973; JANSON & WARD, 
1984), no studies on Littorina have been published showing 
a Mendelian pattern of inheritance for any of the zones 
scored as corresponding to loci. On our gels there are at 
least five regions of activity which we will equate to loci 
for the purpose of discussion (Figure 8a). We did not use 
the esterase data in our phylogenetic analysis; we present 
the qualitative results only. 

The Pgm-1 locus is a compound locus probably rep- 
resenting a recent duplication. The locus was scored as if 
the snails were tetraploid with the alleles of the same 
mobilities present at both loci, something that is commonly 
seen in plants (R. Laushman, personal communication). 
For example in Figure 8b the snails in lanes 5-8 have two 
copies of the allele Pgm-7°*, one copy of Pgm-7'° and one 
copy of Pgm-7'°; the snails in lanes 9-10 have four copies 
of Pgm-7°*; and the snail in lane 11 has two copies of Pgm- 
7'° and two copies of Pgm-7'°*; and the snail in lane 12 
has two copies of Pgm-7°* and two copies of Pgm-7'°. All 
are Littorina subrotundata from Gray’s Harbor, Washing- 
ton. 


Data Analysis 


The allele frequency data were analyzed first using Bio- 
sys-1, release 1.7 (SWOFFORD & SELANDER, 1989). We 
calculated NErs (1972, 1978) unbiased genetic distance. 
We constructed a distance-Wagner tree based on 10 loci 
from 13 operational taxonomic units (= OTUs; FArRIs, 
1981) using SwoFFORD’s (1981) multiple addition crite- 
rion on CAVALLI-SFORZA & EDWARDS’ (1967) chord dis- 
tance. Littorina littorea was used as the outgroup instead 
of Lacuna, as was done in BOULDING (1990b), because L. 
littorea shared the fewest alleles with the other littorinid 
species and because the cladistic analysis of morphology 
for the genus Littorina showed L. littorea was morpholog- 


Page 49 


ically distant from the other littorinid species considered 
here (REID, 1990). 

Bootstrapping was used to obtain confidence limits on 
the validity of different groupings of the OTUs suggested 
in the phylogenies (FELSENSTEIN, 1985). To do this a 
bootstrapping program was written in Turbo Pascal 5.0 
to generate different input files for Biosys-1. Each input 
file contained 10 enzyme loci for all 13 OTUs. The 10 
enzyme loci in the input file were chosen randomly with 
replacement from the 10 original loci for each analysis. 
Thus, in each input file some of the original 10 loci might 
be absent and others might be duplicated. For example 
the first bootstrap run of Biosys-1 might have used Aat- 
1, Aat-1, Sdh-4, Pgm-1, Pgm-1, 6-Pdg, 6-Pdg, 6-Pdg, Pep- 
3, and Gpi, whereas the second run might have used Pep- 
2, Pep-3, Pep-3, Pep-3, Sdh-4, Sdh-4, Pgm-1, Gpi, Gpi, 
and 6-Pdg, and this was continued until 100 runs had been 
made. The output from these 100 runs was then examined 
and a tally was made of the number of times certain groups 
of OTUs appeared together. For the distance-Wagner 
analysis, the cluster was considered discrete if the distance 
between the two groups was at least twice that of the 
distance between any two OTUs in the group. When a 
group of OTUs appeared clustered together at least 95 
times out of 100 during the bootstrapping, this was taken 
as significant support for that grouping in the original 
phylogeny. Some OTUs changed branching orders and 
distances between nodes on more than 5% of the bootstrap 
replicates; this meant that portion of the tree was not fully 
resolved by our data. 


RESULTS 


Field Characters of Littorina from the 
Northeastern Pacific 


Our culture experiments and allozyme data allowed us 
to identify several characters that in combination allow 
separation of these taxa in the field. The shell of Littorina 
sp. either lacked spiral sculpture (Figure 1a, g-i), or had 
a few spiral grooves (Figure 1d), or occasionally had spiral 
sculpture consisting of shallow, evenly spaced, undulating, 
spiral ridges more than twice the width of the grooves 
between them. The shell of L. sitkana could be smooth 
(Figure le) but usually had deep spiral ridges that were 
unevenly spaced and were less than twice as wide as the 
intervening grooves, and often had small riblets in the 
grooves and on the large ridges (Figure 1b). The shell of 
L. sitkana (Figure 1b, e) typically was lower spired (shell 
width 0.86 of shell length) than that of L. sp. The shell 
of L. “kurila” (Figure 1c, f) from Adak Island was typically 
larger than that of L. sp. and had a higher spire. The 
operculum of L. sp. appeared light tan on a live animal 
whereas the opercula of L. sitkana and of L. “kurila” ap- 
peared dark. 

Color differences were also noticeable on the body. Lit- 
torina sp. had cephalic tentacles that were yellow or light 
gray with a dark gray line along the edge above the eye 


Page 50 The Veliger, Vol. 36, No. 1 


Figure 1 


Specimens of Littorina sp. (a, g, h, i), L. sitkana (b), and L. “‘kurila” (c) collected in the field. Specimens of L. sp. 
(d), L. sitkana (e), and L. “kurila” (f) cultured at Friday Harbor for one generation from parents collected in the 
field. Specimen (a) is L. sp. SL = 5.6, SB = 5.3, SW = 5.0, AH = 3.9, AW = 3.2 USNM 860183; specimens (g, 
h, 1) are three additional specimens of L. sp. USNM 860184: (g) SL = 6.6, SW = 6.0, (h) SL = 5.9, SW = 5.5, 
(i) SL = 5.0, SW = 4.3. SL is greatest shell length with one jaw of caliper on apex, SB is greatest shell breadth 
from outer lip of aperture, SW is shell width taken perpendicular to length, AH is greatest aperture length, and 
AW is aperture width perpendicular to aperture length; all measurements were taken with digital calipers in 
millimetres. The smooth L. sitkana (e) was cultured to adult size at a high growth rate in our “tank treatment” 
from parents that had deep spiral ridging as shown by specimen (b). 


E. G. Boulding et al., 1993 


Page 51 


Figure 2 


Measurements made on shells digitized with video digitizing system. a. Measurements taken on axial view. b. 
Measurements taken on apertural view. SL = shell length; SW = shell width; WW = distance between sutures of 
whorl above body whorl; PA (circled) = point of adhesion (of aperture to body whorl); AL = aperture length; AW 
= aperture width; shaded area = AA, area of outer aperture. Dots indicate points used for calculating apical angle; 


see text. 


and dark gray pigment on the head. The pigmentation of 
its tentacles was slightly darker in larger animals. The 
sides of its foot were yellow, and the sole was pale. In 
contrast L. “kurila” had black cephalic tentacles and the 
sides of its foot were black; male L. “kurila’? had black 
pigmentation on the dorsal side of the penis. The body of 
L. sitkana was also dark with black cephalic tentacles and 
black pigmentation on the dorsal side of the penis. Some 
tall-spired L. sp. resembled L. scutulata but the outer lip 
of the aperture of L. scutulata joined the body whorl at an 
angle of less than 45 degrees (cf. Figure 2a) and the penis 
of male L. scutulata had a distinct hooklike filament near 
the end (Murray, 1979). 

The egg masses of Littorina sitkana were larger and had 
a less viscous jelly than did those of L. sp. There were also 
differences in mean adult body size. Whereas it was rare 
to find a L. sp. larger than 5 mm in the field, L. sitkana 
had a mean adult size of 9 mm or larger (Boulding & Van 
Alstyne, in review). The L. “kurila” collected at Adak were 
mostly over 9 mm in height. 

Shell color and pattern was also useful in distinguishing 
these taxa. Common color morphs of Littorina sp. included 
dark brown to olive throughout (Figure 1h); gray to white 
throughout (Figure 1i); dark brown to olive to orange 
background with a narrow white to orange band(s) just 
abapical of the widest part of the last (body) whorl (Figure 
1g); brown to olive to light gray background with dark 


brown stripes, often with a narrow white to orange band 
just abapical of the widest part of the last whorl (Figure 
la, d); and purple to pinkish background with white stripes. 
The shell of L. sttkana was usually dark black-brown to 
dark olive throughout but a common variant had alternate 
white and black bands. Completely white L. sztkana were 
sometimes found. The shell of L. “kurila” on Adak Island 
was usually dark brown or gray and often had dark brown 
spiral stripes. 


Multivariate Analysis of Shell Shape 


The most interesting result from this analysis was that 
the amount of within-taxon variation in shell shape could 
exceed that typically observed between taxa. The ratios of 
whorl width at suture to shell length, and of square root 
of aperture area to shell length were similar among shells 
of field Littorina sitkana, tank L. sitkana, dish L. ‘‘kurila,” 
field L. “‘kurila,” dense L. sp., and field L. sp. (Table 3). 
However, the shells of L. sp. from the sparse treatment 
were appreciably narrower with narrower apertures and 
consequently smaller apertural areas (Table 3). They also 
weighed significantly less (ANCOVA, P < 0.05, covariate 
SL x SW x SW) than their siblings in the dense treat- 
ment. The field L. sitkana weighed significantly more than 
the other six treatments (ANCOVA, P < 0.06, covariate 
SL x SW x SW). 


Page 52 The Veliger, Vol. 36, No. 1 
Table 3 
Means, standard deviations, and mean ratio to shell length of morphometric 
variables used in multivariate analyses of Littorina species. 
L. sitkana L. “kurila” L. sp. 
Tanks Field Dishes Field Sparse Dense Field 
n 25 39 30 36 37 47 33 
Means 
SL 6.56 8.97 5.89 9°55 6.43 4.57 DoD) 
SW eit 7.74 5.14 129 4.41 3.85 4.77 
WW 2.23 2.99 1.98 3.21 1.89 1.59 4.87 
AL 4.81 6.49 4.11 6.45 4.18 3.01 3.86 
AW 3.89 5.30 S515) Suli2 3.04 2.58 3.28 
AA®* 13.31 25.03 10.65 22.42 7.84 5.68 9.32 
Standard deviations 
SL 1.48 1.62 1.38 0.85 0.83 0.52 1.39 
SW UST 1.19 1.14 0.68 0.56 0.45 0.76 
WW 0.51 0.58 0.42 0.26 0.29 0.18 0.35 
AL 0.95 1.08 0.96 0.71 0.53 0.37 0.65 
AW 0.84 0.88 0.90 0.58 0.43 0.30 0.55 
AA®° 5.76 1293) 5.49 5.26 2.05 1685) 3.72 
Ratios 
SL 1.00 1.00 1.00 1.00 1.00 1.00 1.00 
SW 0.88 0.86 0.87 0.76 0.68 0.84 0.83 
WW 0.34 0.33 0.34 0.34 0.30 0.35 0.33 
AL 0:73 0.72 0.70 0.64 0.65 0.66 0.67 
AW 0.59 0.59 0.60 0.54 0.47 0.56 0.57 
AA®> 0.56 0.56 0.55 0.50 0.44 0.52 0.53 


The first stepwise discriminant analysis of only the three 
field treatments selected a classification function consisting 
of the variables shell length (SL), shell width (SW), ap- 
erture length (AL), and aperture area (AA; Table 4). The 
jackknifed classification function correctly classified 92% 
of the Littorina sitkana, 89% of the L. “kurila,” and 91% 
of the L. sp. into the correct group (Table 4). The plot of 
the first and second canonical variables shows almost com- 
plete separation of the field L. sitkana (1) from the field L. 
sp. (A) and partial separation of the field L. “kurila” (U) 
from the other two groups (Figure 6). 

A subsequent analysis including all seven groups yielded 
a discriminant function containing the variables shell length, 
shell width, and aperture length (Table 5). This classifi- 
cation function varied in its ability to correctly classify 
specimens from a high of 94% for the sparse Littorina sp. 
to a low of 37% for the dish L. “kurila” (Table 5). The 
misclassifications were not necessarily into another treat- 
ment of the same taxa (BOULDING, 1990b). The plot of 
the first two canonical variables separated out the sparse 
L. sp. (1) and partially separated field L. sitkana (1) from 
the other six groups along the axis of CV1. The dense L. 
sp. (D) was separated from the field L. “kurila” (U) along 
the axis of CV2 (Figure 7). 

As is typical in discriminant analyses, the composition 
of the canonical variables was very different for the three 
group and the seven group analyses. The standardized 
coefficients for CV1 for the canonical variate analysis for 


the three field taxa were large and positive for shell width 
and aperture length, and large and negative for shell length 
and aperture area (Table 4). The standardized coefficients 
for CV1 from the canonical variate analysis for all seven 
treatments were large and positive for shell width and large 
and negative for shell length (Table 5). The standardized 
coefficients for CV2 for the three taxa analysis were large 
and positive for shell length and smaller and positive for 
shell width (Table 4). The standardized coefficients for 
CV2 for the seven treatments were large and negative for 
shell width and smaller and positive for shell length and 
aperture length (Table 5). In no case was the rank order 
of the groups along the axis of a canonical variable cor- 
related with their mean size (as determined by shell length). 


Shell Sculpture 


The Littorina sitkana grown at high growth rates in the 
tank treatment were either completely smooth or had only 
one to a few ridges abapical to the widest part of the last 
whorl. This occurred even though these snails all had 
parents with deep spiral ridging. Some smooth L. sitkana 
were also collected from the field at Tatoosh Island and 
at other locations. 

Littorina sitkana cultured in dishes at low densities were 
also often smooth even though their field-collected parents 
had had deep spiral ridging. Eleven out of 21 L. setkana 


juveniles from Tatoosh that were isolated in pairs and then 


E. G. Boulding et al., 1993 


Page 53 


Table 4 


Discriminant analysis of field collected snails of three Lit- 
torina taxa: L. sitkana, L. “kurila,” and L. sp. 


Classification function 


Group L. sitkana  L. “kurila” L. sp. 
% correctly classified 92% 89% 91% 
Variable 
In(SL) 26.72 92.99 3392 
In(SW) 416.10 Sind 347.25 
In(AL) 419.94 384.37 344.80 
In(AA°°) — 365.30 — 355.45 — 332.46 
Constant —266.08 —258.93 —202.71 


Standardized coefficients for canonical variables 


Can. Can. 
var. 1 var. 2 
Variable 
In(SL) —161 = 3);118} 
In(SW) 2.11 1.79 
In(AL) 2.56 0.30 
In(AA°*) — 230) 0.47 
Constant —14.99 8.67 


cultured in dishes were completely smooth and the rest 
had weak sculpture. Twenty-three pairs of juveniles from 
San Juan Island that were isolated in dishes grew up to 
be smooth even though their field-collected parents had 
been strongly ridged. Ten L. sitkana whose parents had 
been deeply ridged when collected from Hoonah, Alaska, 
grew up to be completely smooth when grown in pairs in 


culture dishes. Juvenile L. sitkana grown more slowly at 
higher densities were more likely to be ridged. 

Littorina sp. were grown at a range of densities at dif- 
ferent times of the year. Some L. sp. developed fine ridges 
when grown slowly but no L. sp. ever attained the deep 
spiral ridging that is typical of L. sitkana collected in the 
field. When present the ridges of cultured L. sp. were 
evenly spaced and more than twice the width of the grooves 
between them, whereas the ridges of cultured L. setkana 
were unevenly spaced and less than twice as wide as the 
intervening grooves. 


Aperture 


Littorina sp. from the sparse treatment had a narrower 
aperture for its size than L. sp. from the dense treatment, 
the latter being similar in width to L. sitkana (Table 3; 
ANCOVA with shell length as covariate, P < 0.05). The 
inner lip of the L. sztkana aperture is more flared towards 
the base of the columella than is that of L. sp., such that 
there is a greater difference between the outer area (as 
measured; Figure 2b) and the inner area (which the oper- 
culum closes). 


Size 


Littorina sitkana reached sexual maturity at a larger size 
(shell length: females 5.5-7.0 mm, males 4.2-6.0 mm) than 
L. sp. (females 3.8-5.5 mm, mean = 5.25 [SD 0.47]; males 
3.3-5.0 mm, mean = 4.85 [SD 0.52] n = 137). Preliminary 
data suggested that when raised at Friday Harbor, L. 
“kurila” became mature at a greater shell length than the 
other two taxa (females about 6.0 mm, males about 4.8 
mm). 


Table 5 


Discriminant analysis of all seven groups of snails (Littorina). 


Classification function 


Group L. sitkana 

Tanks Field 

% correctly classified 56% 82% 
Variable 

In(SL) 79.5 82.1 

In(SW) 105.0 113.7 

In(AL) —114.1 W223 

Constant —78.5 —102.3 


Standardized coefficients for canonical variables 


Can. Can. 
var. 1 var. 2 

Variable 
In(SL) —2.55 1.18 
In(SW) 3.00 —2.04 
In(AL) 0.07 1.67 
Constant —4.43 —6.85 


L. “kurila” L. sp. 

Dishes Field Sparse Dense Field 
37% 86% 94% 83% 51% 
96.7 146.4 UTS }) 124.7 119.9 
113.1 74.5 —17.4 94.4 90.6 

—77.3 Ay —80.2 — 67.4 —76.3 

= 77/33) =A —80.2 Ooo) = 16:3 

Can. 
var. 3 

—2.40 

ile 3S 
3.45 
9.64 


Page 54 


Animal 


Males of all three taxa had a thick penis with a dorsal 
sperm groove, and a row of mammilliform glands along 
the convex edge nearly to the tip. The penis of Littorina 
sp. was yellow with 7-11 mammilliform glandular papil- 
lae in a single row, a dorsal sperm groove, and a short tip 
(Figure 3c). In general the number of penial glands in- 
creased with body size within any taxon. Sexually mature 
L. sitkana males had between 7 and 18 glands with a mean 
of 13 (shell lengths 6.0-10.0 mm, n = 13). The largest L. 
sitkana found (shell length 25 mm) had 22 penial glands 
arranged in two rows. Littorina sp. males had between 7 
and 11 glands with a mean of 9 (shell lengths 3.5-5.0 mm, 
n = 11). Littorina “kurila” males had between 15 and 17 
glands (shell lengths 4.8—6.4 mm, n = 3). Foot area mea- 
sured by photographing the snail while it was crawling 
on a inverted petri dish was significantly greater for L. sp. 
than for L. sitkhana (ANCOVA, P < 0.007, covariate = 
[SL x SW x SW]®S). 


Reproduction 


These snails all have an egg capsule surrounding a single 
egg (Figure 4a-c). The egg capsule of Littorina sitkana has 
a thick-walled side and a_ thin-walled side 
(BUCKLAND-NIcks & Cui, 1990; Figure 4a, d) but the 
capsules of L. sp. and L. “kurila” have walls of equal 
thickness all the way around (Figure 4b, c, e). Littorina 
sitkana frequently lays communal egg masses which can 
reach 100 mm in diameter whereas L. sp. never does. 
Indeed a large L. sp. will frequently lay several small egg 
masses in quick succession. The egg masses of L. “kurila” 
are similar in size to those of L. sp. The time to hatching 
and the color changes of developing L. sztkana are very 
similar to those of L. sp., and both species have only one 
egg per egg capsule (BUCKLAND-NICKS et al., 1973; Boul- 
ding, unpublished data). 


Radula 


All these snails have very similar radulae (Figure 5). 
The outer marginal teeth in Littorina sitkana had 7 or 8 
cusps (n = 5) (see also ROSEWATER, 1979), those of L. 
“kurila” had 6 or 7 cusps (n = 2) and those of L. sp. 9 or 
10 cusps (n = 5). The lower edge of the base of the ra- 
chidian is not as deeply scalloped for L. sitkana as for L. 
sp. (Figure 5a, b). 


Geographic Ranges 


The confirmed geographic range of Littorina sp. is from 
Sealion Rocks, Sitka, Alaska (57°03’N, 135°20’W) to at 
least as far south as Cape Argo, near Coos Bay, Oregon 
(43°N, 124°W), based on live specimens examined by E. 
G. Boulding. We suspect L. sp. extends as far north as St. 
Lawrence Island (62°50'N, 169°50’W), based on shells 
examined by E.G.B. at the U.S. National Museum 
(USNM) during July 1990. 


The Veliger, Vol. 36, No. 1 


In contrast, Littorina sitkana has a range from northern 
Japan to the Aleutian Islands (REID & GOLIKov, 1991) 
south to Charleston, Oregon (BEHRENS YAMADA, 1977a, 
b). Littermma “kurila” has a range from St. Paul’s Island 
(57°00'N, 171°00'W) and from Akutan Pass (54°00’N, 
166°00’W) through the Aleutian Islands (based on spec- 
imens examined by E.G.B. at the USNM) to the southern 
Kurile Islands (as L. subrotundata in REID & GOLIKOV, 
1991). Thus the ranges of L. sp. and L. “kurila” may 
overlap in the Aleutian Islands, but this is difficult to 
confirm when only shells are available. 


Hybridization Experiments 


In the first experiment, none of the 95 dishes with one 
unsexed Littorina sitkana and one unsexed L. sp. produced 
fertile eggs, while 44% of the unsexed L. sp. x L. sp. did 
so (BOULDING, 1990b). Some of the unsexed L. sitkhana X 
L. sp. crosses laid infertile eggs that failed to develop but 
infertile eggs were also laid by isolated, virgin, adult fe- 
males. 

In the second experiment, fertile eggs were produced 
when northern Littorina sitkana from the Aleutians were 
crossed with southern L. sitkana from Oregon (Table 6). 
All other crosses done between different populations of L. 
sitkana also gave rise to fertile eggs (Table 6). None of the 
four dishes with a female L. sp. from Tatoosh and a male 
L. “kurila” from Adak produced eggs (Table 6). 


Allozyme Electrophoresis 


Allozyme variability: On Tatoosh Island Littorina scu- 
tulata (h = 0.177) had a higher mean heterozygosity per 
locus than L. sztkana (h = 0.007) or L. sp. (h = 0.070). 
The mean sample sizes per locus were 29.5, 36.9, and 40.8 
respectively. 


Diagnostic loci for differentiating Littorina sitkana and 
L. sp.: On Tatoosh Island (Table 1) there are fixed or 
nearly fixed differences at four loci between L. sitkana and 
L. sp. (Table 7). At the Gpi-1 locus, L. sp. is nearly fixed 
for a slower allele than L. sitkana, at the Sdh-4 locus L. 
sp. is nearly fixed for a faster allele than L. sitkana, at the 
Pep-3 locus L. sp. is fixed for a slower allele than L. sitkana, 
and at the Pgm-1 locus L. sp. does not share alleles with 
L. sitkana (Figure 8b, Table 7). Indeed Sdh-4 is probably 
a tetramer and heterozygotes appear as streaks in L. scu- 
tulata, which clearly has several alleles. In L. sitkana we 
saw only a few streaks for Sdh-4 and no homozygotes for 
the Sdh-4'° allele fixed in L. sp. (Table 7); we were not 
sure if these steaks were really heterozygotes but we scored 
them to be conservative. 

We also doubt that the 100 allele for Gpi-1 is really 
present in the Littorina sp. population at Tatoosh; an allele 
with a frequency of 0.01 would be expected to be present 
almost exclusively in heterozygotes (see DOBZHANSKY ef 
al., 1977); yet we never saw the clear three banded pattern 
for any L. sp. individual that we saw in L. scutulata het- 
erozygotes for Gpi-1. 


E. G. Boulding et al., 1993 


Page 55 


Figure 3 


Scanning electron micrograph (SEM) of penes of three taxa (Littorina) showing number and arrangement of penial 
glands (PG). Arrowheads indicate dorsal sperm groove. a. L. “kurila,” b. L. sitkana, and c. L. sp. 


There was a rare allele slower than the 100 allele at 
the 6-Pgd locus that was present for Littorina sp. and not 
for L. sitkana, and another rare allele slower than the 100 
allele at the Pep-2 locus that was present for L. sp. but 
not for L. sitkana. 


The value of Nei’s unbiased genetic identity obtained 
for Littorina sitkana and L. sp. was 0.63 for the 10 loci 
assayed for all OTUs (Table 8). Four loci—Sod-S, Sod- 
F, Mdh-S, and Lap-S—were observed to be monomorphic 
for both L. sitkana and L. sp. These data were included 


Page 56 The Veliger, Vol. 36, No. 1 


Sum 


ast, axe 
« \ a Oe at ie 


Egg capsule morphology of the three taxa (Littorina). All eggs were laid at Friday Harbor Laboratories. a. Two 
egg capsules of L. sitkana from Tatoosh Island each containing an embryo. Tk indicates thick side of capsule and 
Tn indicates thin side. b. Egg capsule of uniform thickness of L. sp. from Tatoosh Island. c. Egg capsules of uniform 
thickness of L. “kurila” from Adak. d. Light micrograph of a 1 um section through an egg mass of L. sitkana viewed 
with Nomarski optics. Note that egg capsule wall has a thick side (Tk) and a thin side (Tn). Y marks the yolk 
and A marks the albumen, which is patchy and has shrunk back from the egg capsule wall. The dark region 
between the capsules is the jelly matrix in which the capsules are embedded. e. Light micrograph of 1 wm section 
through an egg mass of L. sp. Note thin capsule wall relative to d. 


E. G. Boulding et al., 1993 


Figure 5 
SEM of radulas of the three Littorina species. a. L. “kurila,” b. 
L. sitkana, c. L. sp. Note that the central tooth (rachidian) is 
narrowest and most pointed in L. sztkana, intermediate in L. sp. 
and most blunt in L. “kurila.”” The number of cusps on the outer 


marginal teeth varies from about 6 or 7 for L. “kurila,” to 7 or 
8 for L. sp., and 9 or 10 for L. sitkana. 


Page 57 


in a separate run of Biosys-1 making the total number of 
loci 14; this gave a value of Nei’s unbiased genetic identity 
of 0.74 and a value of Cavalli-Sforza and Edwards’ chord 
distance of 0.46. 

The esterase phenotype was also useful in distinguishing 
Littorina sitkana and L. sp. (Figure 8a). The Est-3 band 
was closer to the Est-2 band for the L. sitkana than for L. 
sp. The patterns at the darkly staining Est-5 region also 
were different but were even more difficult to score. The 
L. sp. has some common alleles for the Est-5 region that 
are faster than any present for L. sitkana from Tatoosh 
(Figure 8a). 


Intraspecific relationships: Of the four populations of 
Littorina sitkana surveyed for all 10 loci, the Mukkaw Bay 
population and the Oregon population were similar to the 
Tatoosh population in being fixed for the 100 allele at the 
Gpi-1, Sdh-4, and Pgm-1 loci. These same loci were also 
fixed for the 100 allele in the Hoonah and Whitestone 
populations of L. sztkana (Table 1). However, the Adak 
population of L. sitkana differs in having about equal num- 
bers of the Sdh-4'° and Sdh-4'° alleles and in being fixed 
for a faster allele for the Pgm-1 locus (Table 7). The L. 
sitkana population from Oregon was unique in being fixed 
for a single band in the Est-5 region and at the Est-3 
region (Figure 8a) and also in showing no variation at any 
of the other 10 loci surveyed (Table 7). 

The two populations of Littorina sp. that were surveyed 
for all 10 loci (Table 7) and the Shi Shi (n = 3) population 
were similar in being fixed or nearly fixed for Gpi-7°° 
allele and the Sdh-4'% allele. 


Interspecific relationships: Littorina littorea and L. ob- 
tusata were the most different from the other Littorina 
OTUs (Table 7). All the Littorina OTUs were fixed for 
the 100 alleles at the 6-Gala and B-Ga loci except for L. 
obtusata. Littorina littorea and L. scutulata had unique al- 
leles at the Pgm-1 locus. Littorina scutulata had unique 
alleles at the Sdh-4 locus that were not shared by any of 
the other OTUs. All the Littorina OTUs were fixed or 


Table 6 


Results of attempted crosses between Littorina sitkana and L. sp. from different populations. Only fertile eggs produced 
between 31 August 1988 and 31 August 1989 are noted. All females were virgin when confined with the male. Fractions 
refer to number of crosses producing fertile eggs out of number of crosses attempted. 


Male species L. sp. L. sitkana 
Site!: Tatoosh Tatoosh Adak Siletz Attu Hoonah 
Female species Site 

L. sp. Tatoosh 19/20? 0/2? 
L. sitkana Tatoosh 0/42 4/4 1/2 4/4 1/1 
L. sithana Adak 1/2 2/6 1/3 
L. sithana Siletz 2/5 2/4 2/4 2/3 
L. sitkana Attu 
L. sitkana Hoonah 3/4 2/2 


' Site locations are specified in Table 1. 
2 See text for more information. 


Page 58 The Veliger, Vol. 36, No. 1 


Table 7 


Allele frequencies in Littorina populations sampled. 


Population! 
si si SI Si sax ob sp sp ku sub sub lit sc Lac 
Ta Al Mk OR RI RI Ta Ba Al Mk Gh RI Ta Fh 
Locus 
6-Pgd 
(n) 12 3 3 3 10 16 18 5 6 5 12 11 7 4 
88 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.73 0.00 0.00 
92 0.00 0.00 0.00 0.00 0.00 0.00 0.03 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
100 1.00 1.00 1.00 1.00 0.85 1.00 0.97 1.00 1.00 1.00 1.00 0.27 0.93 0.00 
104 0.00 0.00 0.00 0.00 0.10 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
110 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.07 0.00 
112 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.50 
114 0.00 0.00 0.00 0.00 0.05 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
122 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.50 
Pep-3 
(n) 27 10 3 2 20 23 26 5 5 13 12 20 17 6 
96 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
98 0.00 0.00 0.00 0.00 1.00 0.00 1.00 1.00 1.00 0.04 0.00 0.00 0.00 0.00 
100 1.00 1.00 1.00 1.00 0.00 0.00 0.00 0.00 0.00 0.96 1.00 0.00 1.00 0.00 
104 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.00 
106 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.00 
Pep-2 
(n) 48 3 12 12 30 29 60 6 15 26 10 12 55 4 
60 0.00 0.00 0.042 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
92 0.00 0.00 0.00 0.00 0.00 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
100 1.00 1.00 0.96 1.00 1.00 1.00 0.99 1.00 1.00 1.00 1.00 1.00 0.97 0.00 
106 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.37 1.00 
Gpi-1 
(n) 116 10 10 32 24 26 43 6 22 19 21 29 56 4 
86 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.09 0.00 
90 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.25 0.00 
92 0.00 0.00 0.00 0.00 0.00 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
94 0.00 0.00 0.00 0.00 0.00 0.19 0.00 0.00 0.00 0.00 0.00 0.00 0.66 0.00 
96 0.00 0.00 0.00 0.00 0.04 0.77 0.98 1.00 1.00 1.00 1.00 0.00 0.00 0.00 
100 1.00 1.00 1.00 1.00 0.96 0.04 0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
106 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.25 
112 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.75 
Aat-1 
(n) 43 6 3} 19 12 10 39 3 13 5 3 8 38 4 
100 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 0.00 
108 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.00 
B-Gala 
(n) 15 4 1 3 16 17 17, 6 5 9 14 17 12 3 
100 1.00 1.00 1.00 1.00 1.00 0.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 0.00 
108 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
130 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.00 
B-Ga 
(n) 20 6 3 3 21 15 25 6 7 12 17 16 12 4 
100 1.00 1.00 1.00 1.00 1.00 0.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 0.00 
112 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
116 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.00 
Sdh-4 
(n) 67 10 7 38 22 11 22 5 21 25 12 21 50 3 
100 0.96 0.45 1.00 1.00 0.16 0.00 0.02 0.00 0.00 0.00 0.17 1.00 0.00 0.00 
108 0.04 0.55 0.00 0.00 0.84 1.00 0.98 1.00 1.00 1.00 0.83 0.00 0.00 0.00 


114 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.29 0.00 


E. G. Boulding e¢ al., 1993 Page 59 
Table 7 
Continued. 
Population! 
Sl si sl si sax ob sp ku sub sub lit sc Lac 
Ta Al Mk OR RI RI Ba Al Mk Gh RI Ta Fh 
120 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.59 0.00 
124 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.33 
126 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.12 0.00 
130 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.67 
Sdh-1 
(n) 14 10 2 2 36 Si 2 4 2 2 22 30 0 
100 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 — 
Pgm-1 
(n) 1 11 14 3 30 29 10 12 26 25 30 18 8 
74 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.50 0.00 
77 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.33 0.50 0.00 
86 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.67 0.00 0.00 
94 0.00 0.00 0.00 0.00 0.00 0.00 0.05 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
96 0.00 0.00 0.00 0.00 0.03 0.35 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
98 0.00 0.00 0.00 0.00 0.97 0.65 0.60 1.00 0.00 0.61 0.76 0.00 0.00 0.13 
100 1.00 0.00 1.00 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 
102 0.00 0.00 0.00 0.00 0.00 0.00 OBZO O00 0:58 0:27 0.12 0.00 0.00 0.87 
104 0.00 1.00 0.00 0.00 0.00 0.00 0.05 0.00 042 O12 O12 0.00 0.00 0.00 


' Key to populations: si Ta = L. sitkana Tatoosh; si Al = L. sitkana Aleutian Is.; si Mk = L. sttkana Mukkaw; si OR = L. sitkana 
Oregon; sax RI = L. saxatilis Rhode Is.; ob RI = L. obtusata Rhode Is.; sp Ta = L. sp. Tatoosh; sp BA = L. sp. Bamfield; ku Al = L. 
“rurila” Aleutian Is.; sub Mk = L. subrotundata Mukkaw; sub Gh = L. subrotundata Grays Harbor; lit RI = L. littorea Rhode Is.; sc 


Ta = L. scutulata Tatoosh; Lac Fh = Lacuna Friday Harbor. 


nearly fixed for the 100 allele at the 6-Pdg locus, whereas 
L. littorea had only a low frequency of the 100 allele. 

Lacuna was too distantly related to be a good outgroup; 
it shared alleles with other OTUs only at the Pep-2 locus 
(with Littorina scutulata), and the Gpi-1 locus (with Lit- 
torina littorea), and at the Pgm-1 locus (with the Littorina 
subrotundata) (Table 7). Therefore we used Littorina lit- 
torea as an outgroup for our analysis even though BOULDING 
(1990b) had previously used Lacuna as the outgroup. 

The distance-Wagner tree constructed using CAVAL- 
LI-SFORZA & EDWARDS’ (1967) chord distance is shown 
in Figure 9. For all species the absolute distances of the 
OTUs from the root varied considerably under different 
bootstrap runs. Littorina scutulata was consistently distant 
from all other OTUs and consistently branched off the 
phylogeny just after L. littorea. Littorina obtusata was con- 
sistently distant from all other OTUs and especially distant 
from L. littorea, but its position of attachment onto the 
phylogeny was not robust under bootstrapping. 

There was a cluster made up of Littorina sitkana pop- 
ulations from Tatoosh, Mukkaw, and Oregon that was 
robust under the bootstrapping. The L. subrotundata from 
Grays Harbor and from Mukkaw Bay often formed a 
distinct cluster but sometimes clustered with L. sp. and L. 
“kurila.” The L. sp. from Bamfield and from Tatoosh 
clustered together most of the time but often L. saxatilis or 
L. subrotundata moved into the cluster. 


The Littorina sitkana from Adak Island in the Aleutians 
shared alleles with the L. sztkana cluster and also with the 
L. sp. cluster. 

The Littorina subrotundata from Mukkaw and the L. 
subrotundata from Grays Harbor did not form a group that 
was significantly distinct from the L. sp. from Tatoosh and 
Bamfield. Littorina subrotundata from both locations were 
fixed for the 100 allele while L. sp. was fixed for the 98 
allele at the Pep-3 locus (Table 7). We scored one 98 allele 
in one L. subrotundata individual near the edge of the gel 
but we think this is an error. The 98 and 100 alleles of 
Pep-3 were a maximum of 2 mm apart so they could not 
be distinguished on some gels and were not distinguished 
in BOULDING (1990b). We eliminated all the Pep-3 data 
from any gel that was not run long enough to distinguish 
the 98 and 100 alleles. This resulted in smaller sample 
sizes for this locus but enabled us to include data from 
these alleles (Table 7). These two alleles could be distin- 
guished more consistently in future studies if the gels were 
run longer or perhaps by changing the pH of the buffer. 

Littorina saxatilis and L. sp. could be distinguished by 
a nearly fixed difference at the Gpi-1 locus (Table 7). 
They also had different allele frequencies and some unique 
alleles at the Sdh-4 and Pgm-1 loci (Table 7). 

Nei’s genetic identity for Littorina sp. from Tatoosh and 
L. “kurila” from Adak is 0.971 (Table 8) for the 10 loci 
assayed for all OTUs. Most of the difference is at the 


Page 60 


4.0 


0.0 


variable 2 


canonical 


-4.0 


-4.0 


The Veliger, Vol. 36, No. 1 


0.0 4.0 


canonical variable 1 


Figure 6 


Plot of the first canonical variable (CV1) against the second canonical variable (CV2) for the first discriminant 


with adult snails (Littorina) collected from the field only. Centroids for each group are as follows: U = L. “kurila 


”» 


from Adak Island, I = L. sitkana from Tatoosh Island, and A = L. sp. from Tatoosh Island. Outlines are convex 
hulls (curves) surrounding 100% of the points for that group. 


Pgm-1 locus complex where the two taxa have a single 
locus Nei’s genetic identity of 0.417. 


DISCUSSION 
Morphometrics 


An important finding of this study is that the Littorina 
sp. from the sparse treatment, cultured at a density of 10 
juveniles per dish, differed more in shell shape from the 
L. sp. in the dense treatment, cultured at a density of 30 
juveniles per dish, than any of the three species differed 
from each other. This is even more surprising considering 
that each dish in the sparse treatment was paired with a 
dish of full siblings in the dense treatment, so the genetic 
diversity between these two groups was much less than 
between any other two groups in the analysis. This shows 
clearly that multivariate morphometric analyses alone do 
not solve the taxonomic problems of sibling species. Work- 
ers on littorinids and other gastropods should be cautious 
about interpreting separation on a multivariate plot as 
evidence for or against the existence of a sibling species 
(e.g., MURRAY, 1982; WELLINGTON & KurIs, 1983; JANSON 


& SUNDBERG, 1983; JANSON, 1985; JANSON & WARD, 
1985). 

It is important to distinguish differences in size from 
differences in shape in order to identify the shells of juvenile 
littorinids from closely related taxa. Ratios of shell mea- 
surements to shell lengths are used commonly in species 
descriptions and were used by RAup (1961, 1966) in his 
theoretical models of shell shape, but single ratios are not 
as powerful as multivariate analyses for separating sibling 
species (PIMENTAL, 1979; REYMENT ef al., 1984). A ratio 
will not be constant within a group if there is allometry 
(REYMENT et al., 1984) or if there is substantial plasticity. 
Our data show that the ratio of various shell dimensions 
to shell length can vary considerably with growth rate 
(Table 3). 

Canonical variate analysis selects coefficients and vari- 
ables so that a linear combination of the variables is formed 
that best separates the groups (PIMENTAL, 1979; REYMENT 
et al., 1984). A problem with canonical variate analysis is 
that it tends to separate well separated groups further 
without separating poorly defined groups included in the 
same analysis. The three field treatments were better sep- 


E. G. Boulding et al., 1993 


6.0 


N 
& 
fo} 
wo 
= 
is) 
© 0.0 
re 
‘2 
Cc 
eo) 
Cc 
is} 
Oo 
-6.0 


Page 61 


0.0 6.0 


canonical variable 1 
Figure 7 


Plot of CV1 against CV2 for the canonical variate analysis from the second discriminant with all seven treatments 
with Littorina species. Centroids for each group are as follows: U = field L. “‘kurila,’ K = dish L. “kurila,” I = 
field L. sitkana, S = tanks L. sitkana, A = field L. sp., T = sparse L. sp., D = dense L. sp. Outlines are convex 
hulls (curves) surrounding 100% of the points for that group. 


arated along the axis of CV1 in the first discriminant 
analysis (Figure 6) than in the second discriminant anal- 
ysis with all seven groups (Figure 7). The classification 
functions from this first analysis (Table 4) would be most 
useful to other workers trying to classify shells collected 
from the field on the basis of shape alone. 

None of the separation along the axes of the canonical 
variables seemed solely attributable to size (Figures 6, 7, 
Tables 3-5). This was fortunate because differences in 
adult size will not be helpful in separating juveniles of 
these littorinids. SUNDBERG (1988) found that the major 
part of the variation in shell morphology between exposed 
and sheltered populations of Littorina saxatilis could be 
attributed to differences in size. What is of considerable 
interest is whether there is allometry that could result in 
shape differences among different populations solely due 
to differences in mean size (K. Johannesson, personal com- 
munication). An example of this occurred when shape 
differences among two stocks of haddock on a canonical 
variable plot were attributable to differences in mean body 
size between the two samples (MCGLADE & BOULDING, 
1983) which probably resulted from fish of similar ages 
schooling together. 


Variation between species of littorinids must be consid- 
ered in the context of variation within a species, especially 
in species that have direct development and therefore lim- 
ited dispersal. JANSON & WARD (1984) studied microgeo- 
graphical variation in allozyme and shell characters in 
Littorina saxatilis. They found considerable morphological 
variation within one kilometer, especially between exposed 
and sheltered populations, but analysis of the allozyme 
data suggested this was due to within-species variation. In 
the northeastern Pacific, L. sztkana inhabits protected shores 
and L. sp. very exposed shores, but the species co-occur 
in areas of intermediate exposure near very exposed areas 
(Boulding & Van Alstyne, in review); it would be inter- 
esting to look for microgeographic variation of the sort 
described by JANSON & WARD (1984) within each of these 
two species. 


Plasticity in Phenotype 


Phenotypic plasticity in shell form has long been rec- 
ognized by gastropod systematists. For example CAR- 
PENTER (1864:531) synonymized three species of Littorina 
because he found no gaps in shell form in a large series 


Page 62 


hm WN — 


& 
= 


| geee,. « ** a 


a 
4 *e « 


1 4 7 
Figure 8 


a. A photograph of a gel stained for Est a NA. Lane 1 is Littorina sitkana from False Bay, lanes 2 and 3 are L. 
scutulata from Tatoosh, lanes 4 through 8 are L. sitkana from Oregon, and lanes 9 through 15 are L. sp. from 
Tatoosh. Note fixed position of bands for L. sitkana from Siletz Bay, Oregon. These were fixed for all 30 snails 
that were assayed from this population, which is near the southern limit for L. sttkana. b. A photograph of a gel 
run in an AmC 7.0 buffer and stained for Pgm using an agar overlay. Lane 1 is L. sp. from Tatoosh, lanes 2 to 4 
contain L. sitkana from Tatoosh, lanes 5 and 6 contain L. subrotundata from Grays Harbor, then there is a blank, 
and lanes 7 to 12 contain L. subrotundata from Grays Harbor. Note the position of the allele for L. sttkana between 
the slow and medium alleles shared by the other two species (see text for interpretation). c. A photograph of a gel 
stained for SDH. Lanes 1 to 3 are L. sp., lanes 4 to 6 are L. sitkana, and lane 7 is L. saxatilis. Note there are two 
loci shown: 3, which stains faintly, and 4, which stains darkly. The allele Sdh-4'" for locus 4 for L. sp. covers the 
allele Sdh-3'°° for locus 3, whereas for L. sitkana the allele Sdh-4' for locus 4 is slower than the allele Sdh-3'© for 
locus 3. Note the streak for L. saxatilis, which is probably a heterozygote for Sdh-4'°/Sdh-4'". 


The Veliger, Vol. 36, No. 


E. G. Boulding e¢ al., 1993 Page 63 


DISTANCE FROM ROOT 


0.0 0.2 0.4 0.6 
ee ee ee | aa le es | 


L. sitkana Tatoosh 
32 


90 L. sitkana Oregon 


76 L. sitkana Mukkaw 


L. sitkana Alaska 


ou L. saxatilis Rl 


50 L. obtusata RI 
12 L. sp. Tatoosh 
190 34 a L. sp. Bamfield 


L. ‘kurila' Adak, AK 


66 L. subroundata Mukkaw 
L. subroundata Gr Hb 


L. scutulata Tatoosh 


L. littorea Rl 


[jn PELE On an ai na | 
Figure 9 


A distance-Wagner tree constructed using CAVALLI-SFORZA & EDWARDS’ chord (1967) distance using SWOFFORD’s 
(1981) multiple addition criterion and no optimization. The numbers at the branching points represent the number 
of times the OTUs to the right of the branch points occurred as a group in the 100 bootstrapped replicates. Distinct 
for distance-Wagner analysis means that the distance between the groups of OTUs was at least twice that between 
any two OTUs in the group. 


Table 8 


Genetic distance measures between pairs of Littorina populations. Below diagonal: NEI’s (1978) unbiased genetic identity. 
Above diagonal: CAVALLI-SFORZA & EDWARDS’ (1967) chord distance used to construct distance-Wagner tree. 


Population! 1 2 3 4 5 6 7 8 9 10 11 12 13 
1 L. sitkana Ta — 0.312 0.057 0.039 0.453 0.674 0.540 0.555 0.555 0.479 0.443 0.532 0.497 
2 L. sitkana Al 0.871 — 0.331 0.328 0.418 0.641 0.482 0.514 0.460 0.396 0.372 0.555 0.497 
3 L. sitkana Mk 1.000 0.867 — 0.041 0.470 0.687 0.555 0.571 0.571 0.496 0.460 0.533 0.499 
4 L. sitkana OR 1.000 0.868 1.000 — _ 0.468 0.686 0.554 0.569 0.569 0.495 0.458 0.531 0.497 
5 L. saxatilis RI 0.728 0.782 0.721 0.722 — 0.561 0.294 0.281 0.398 0.402 0.404 0.578 0.578 
6 L. obtusata RI 0.427 0.492 0.419 0.422 0.585 — 0.534 0.518 0.578 0.532 0.533 0.725 0.679 
7 L. sp. Ta 0.627 0.700 0.620 0.621 0.890 0.660 — _ 0.146 0.196 0.266 0.303 0.595 0.574 
8 L. sp. Ba 0.606 0.673 0.598 0.600 0.902 0.671 0.988 — 0.285 0.287 0.314 0.602 0.573 
9 L. “kurila” Al 0.622 0.734 0.614 0.616 0.823 0.619 0.971 0.924 — 0.310 0.360 0.602 0.573 
10 L. subrotundata Mk 0.725 0.809 0.718 0.719 0.789 0.666 0.902 0.894 0.874 — 0.101 0.602 0.499 
11 L. subrotundata Gh 0.748 0.815 0.742 0.743 0.790 0.661 0.888 0.891 0.846 0.996 — 0.574 0.497 
12 L. littorea RI 0.655 0.615 0.655 0.656 0.585 0.358 0.572 0.552 0.566 0.570 0.590 — _— 0.577 

13 L. scutulata Ta 0.763 0.781 0.759 0.761 0.658 0.464 0.671 0.650 0.668 0.781 0.788 0.622 — 


' Key to locations: Ta = Tatoosh Island; Al = Adak Island; Mk = Mukkaw Bay, Washington; OR = Siletz Bay, Oregon; RI = 
Rhode Island; Ba = Bamfield; Gh = Grays Harbor, Washington. For more information on locations see Table 1. 


Page 64 


of specimens. Unfortunately the approach of identifying 
species by looking for large breaks in an ordered series of 
forms does not work well for some groups; two of the 
littorinids that Carpenter synonymized are considered by 
Murray (1979, 1982) and MAsTRO et al. (1982) to be 
separate species. 

The range of shell shape and shell sculpture in Littorina 
sp. raised at high and low densities, which resulted in low 
and high growth rates respectively, differs from the range 
seen in L. sitkana cultured at low and high growth rates; 
this suggests significant genetic differences between the two 
taxa. No L. sp. ever developed deep spiral sculpture char- 
acteristic of L. sitkana in the field and no L. sitkana ever 
became as high spired as the L. sp. grown at low densities 
in the dishes or in the tanks. In contrast L. sitkana grown 
at fast growth rates tended to have lower spires than those 
that had grown more slowly. 

Soft part anatomy also has been shown to change with 
ontogeny and with changes in environmental conditions. 
Foot size of a thaidid gastropod has been shown to vary 
with environmental conditions (ETTER, 1988). Variation 
in penial morphology and pigmentation (HANNAFORD EL- 
Lis, 1979; RAFFAELLI, 1979), number of penial glands 
(RAFFAELLI, 1979; JANSON, 1982), number of cusps on the 
outer marginal teeth of the radula (REIMCHEN, 1974), 
bluntness of rachidian teeth of the radula (RAFFAELLI, 
1979), and amount of head pigmentation (JAMES, 1968) 
with size for species in the Littorina saxatilis species com- 
plex makes it difficult to use these characters to distinguish 
between sibling species. 

Penial morphology and the morphology of the bursa 
copulatrix are likely important in species cohesiveness. 
SAUR (1990) found that initiation of copulation occurred 
as frequently with same sex partners as with those of the 
opposite sex but that the duration of copulation was con- 
siderably shorter for intrasexual copulation. She hypoth- 
esizes that sex and species recognition occurs when the 
penis contacts the bursa copulatrix and that this recog- 
nition prolongs copulation. We do not know whether the 
small differences in penial morphology between Littorina 
sitkana and L. sp. (Figure 3) are significant for species 
recognition or whether it is the secretions from the penial 
glands that are important. 


Hybridization and Speciation 


The ability of Littorina sitkana from the north and south 
extremes of the species distribution to interbreed supports 
the classification of L. sztkana as one species in the northern 
Pacific. However, the viability and fertility of the hybrid 
offspring and their ability to backcross with their parents 
would have to be tested before this could be shown con- 
clusively. WARWICK et al. (1990) have reported that while 
male L. saxalilis could be crossed with female L. arcana, 
the reverse was not true; the female hybrid progeny could 
be backcrossed to male L. saxatilis. There are many doc- 
umented cases where male hybrid inviability or sterility 


The Veliger, Vol. 36, No. 1 


develops during the speciation process before female hybrid 
inviability or sterility (for review see DOBZHANSKY et al., 
1977; COYNE & OrR, 1989). So far we have been unable 
to obtain a single offspring from the many reciprocal L. 
sitkana xX L. sp. crosses or the few L. sp. female x L. 
“kurila” male crosses we have tried. Even if we were to 
obtain L. sp. x L. “kurila” hybrids we would have to check 
the fertility of both the male and female hybrid offspring 
before we concluded they were capable of interbreeding. 
One factor that makes crossing the latter two taxa difficult 
is that the L. “kurila” from Adak lays eggs only once a 
year, in late June to early July, whereas L. sp. lays eggs 
all year round. This could be the result of a cline in the 
timing of onset of reproduction; GOLIKOV & KUSSAKIN 
(1978) report that the onset of reproduction becomes later 
in the summer for L. kurila from the northwestern Pacific 
and BEHRENS YAMADA (1989) reports that L. setkana from 
Oregon had different periods of peak reproduction that L. 
sitkana from Friday Harbor. 


Biochemical Systematics 


Allozyme differences among Littorina sitkana, L. sp., 
L. “kurila,” and L. subrotundata: Our electrophoretic 
data show clearly that Littorina sitkana and L. sp. are two 
distinct species. There are fixed or nearly fixed differences 
in allelic allozymes at four loci (Table 7). The presence 
of fixed differences in allelic allozymes between sympatric 
populations is strong evidence that the populations are 
reproductively isolated (FERGUSON, 1980). These two spe- 
cies are sympatric on Tatoosh Island—their distributions 
overlap in areas of intermediate exposure (Boulding & 
Van Alstyne, unpublished data) and they have the oppor- 
tunity to interbreed. But L. sp. is abundant only on ex- 
tremely wave-exposed intertidal shores while L. sztkana is 
abundant only on protected shores (Boulding & Van Al- 
styne, unpublished data). 

Before interpreting unique bands on a gel as evidence 
of absence of gene flow between two sympatric taxa, the 
genetic basis of the banding pattern should first be estab- 
lished (FERGUSON, 1980). WARD ef al. (1986, 1991) have 
done breeding studies to confirm the Mendelian segrega- 
tion of codominant alleles for the enzyme loci Gpi, Aat-1, 
Pgm-1, Pgm-2, and for 10 other loci for Littorina saxatilis. 
DILLON (1986) demonstrated that Gpi, Opdh, and Est 
showed Mendelian inheritance patterns for the freshwater 
snail Goniobasis proxima when held under standard con- 
ditions. 

These results from electrophoresis of allozymes support 
our conclusion from the morphological data that Littorina 
sp. is not conspecific with L. sztkana. Two populations of 
L. subrotundata were fixed for Pep-3'” and two populations 
of L. sp. were fixed for Pep-3°*, which suggests they are 
separate taxa; this result would be more conclusive if we 
had sampled more populations. 

In contrast, the differences in allele frequencies between 
Littorina sp. from Tatoosh and L. “kurila” from Adak 


E. G. Boulding et al., 1993 


Island in the Aleutians might result from a geographical 
cline in allele frequencies (see DOBZHANSKY et al., 1977) 
and does not necessarily mean they should be considered 
different species. Microgeographic clines are also known; 
JOHANNESSON & JOHANNESSON (1989) found a cline in 
the allele frequency of Aat between high- and mid-rocky 
shore populations of L. saxatilis. 

Littorina sitkana from Adak was more similar to L. “ku- 
rila” from Adak (Nei’s genetic identity = 0.73) than L. 
sitkana from Tatoosh was to L. sp. from Tatoosh (I = 0.63 
for same 10 loci). 


Interspecific relationships: In some cases phylogenies from 
allozyme data can provide better resolution than those 
constructed using newer techniques such as restriction en- 
zyme analysis of mtDNA (DOWLING & BRown, 1989) 
although the best resolution may come from direct se- 
quencing of DNA using the polymerase chain reaction 
(INNIS et al., 1988). Considerable literature has been de- 
voted to the merits of one method of constructing phylog- 
enies from distance data over another (see FELSENSTEIN, 
1982; RoGERS, 1986). However, the subsets of OTUs that 
were robust under the bootstrapping were almost the same 
for a UPGMA dendogram we constructed but do not pre- 
sent (BOULDING, 1990b) and the distance-Wagner tree we 
do present (Figure 9). Both trees showed one subset con- 
sisting of Littorina sitkana from Tatoosh, Mukkaw Bay, 
and Oregon and a second less robust subset consisting of 
L. sp. from Bamfield and Tatoosh and L. “kurila” from 
Adak. Littorina scutulata, L. obtusata, and L. littorea were 
only distantly related to the two clusters and to each other. 

The quality of phylogenies at the species level based on 
allozyme data depends mostly on the number of loci sur- 
veyed and is less dependent on the sample size drawn from 
each population (FERGUSON, 1980). This is because in 
interspecific comparisons loci are usually either fixed for 
different allelic allozymes or identical making it unnec- 
essary to estimate precisely allele frequencies (AVISE, 1983). 
Only 10 loci were used in the present study, which allowed 
resolution of parts of the phylogeny dealing with more 
distantly related species but did not allow us to determine 
the exact branching pattern for more closely related species. 

We encountered problems with using bootstrapping to 
put confidence limits on our trees based on allozyme data. 
Two of our enzyme loci, Aat-1 and Sdh-1, were mono- 
morphic for all species that were included in the analysis 
(Table 7). The replicate bootstrap samples that happened 
to get several copies of these monomorphic loci contributed 
to the low scores at several of the branch points (Figure 
9). This was particularly true for branch points between 
species such as Littorina subrotundata and L. sp. These 
were different at only the Pep-3 locus, which is a digestive 
enzyme. The bootstrapping procedure treats all loci equal- 
ly, yet digestive enzymes, such as the esterases and pep- 
tidases, accumulate different alleles at a faster rate than 
enzymes involved in central metabolic processes and are 
therefore more likely to distinguish closely related species 


Page 65 


(see FERGUSON, 1980). Hillis (presentation at SSB meet- 
ing, 1991) has created experimental phylogenies using dif- 
ferent cultures of a phage and reports that 95% confidence 
limits determined by bootstrapping DNA sequence data 
is an overly conservative method of detecting robust group- 
ings of OTUs; he says that groupings that appear together 
70% of the time should be considered robust. 

Comparison of phylogenies constructed from allozyme 
data with those derived from morphological data often 
reveals similarities and differences (HILLIS, 1987). The 
species of littorinids used in this study have been included 
in a phylogeny based on morphological characters (REID, 
1990). Reid’s phylogeny shows Littorina scutulata branch- 
ing off the cladogram, then L. l:ttorea, then L. sitkana, then 
L. “kurila,” then L. obtusata, and finally L. saxatilis. This 
pattern is not really as different from the distance- Wagner 
tree (Figure 9) as first appears. If only the robust branches 
of Figure 9 are considered, then the branching order is 
really only significantly different for L. obtusata, which 
may be more distinct from the L. sztkana cluster and the 
L. sp. cluster than is indicated by Reid. The position of 
L. saxatilis on our phylogeny is not resolved by our allozyme 
data although the data show L. saxatilis is a separate taxon 
from L. sitkana and from L. sp. 


Systematics of Littorina sitkana, 
i@sp»and=Li skunlan 


The differences in shell shape, shell weight and ridging 
under different growth conditions, head and penis pig- 
mentation, egg capsule and spawn morphology, and size 
at maturity demonstrate that Littorina sitkana and L. sp. 
are separate species. ‘Their failure to hybridize supports 
this conclusion. The electrophoretic data showed that these 
two species are fixed or almost fixed for different alleles 
at four loci, Pgm-1, Gpi-1, Pep-3 and Sdh-4, and that 
they have different banding patterns for Est a NA. 

If only field-collected adult snails from three taxa are 
considered, then additional snails from these populations 
could be assigned to a taxon with a reliability of about 
90% using our discriminant function on their shell shape 
measurements. Of course if data on shell ridging or soft 
part pigmentation were included, the reliability would be 
much higher. The use of the field characters described here 
has made it possible to tell the two species apart 100% of 
the time. 

Littorina sp. shows a number of genetic differences from 
L. “kurila” in the light pigmentation of its head, its un- 
pigmented penis, and in the timing of its reproductive 
period, and may be a separate taxon. The differences in 
pigmentation were heritable. We observed differences in 
behaviors adapting L. sp. to wave-exposed habitats, such 
as its rapid emergence from its shell when dislodged and 
its rapid subsequent readhesion to the substrate (Boulding 
& Van Alstyne, unpublished data), not seen in the L. 
“kurila” collected from Adak or in their offspring cultured 
at Friday Harbor Laboratories. Alternatively L. “kurila” 


Page 66 


and L. sp. may represent the north and south ends of a 
geographic cline. Only more extensive collections from 
Alaska and the Aleutian islands can resolve whether L. 
“kurila” and L. sp. are separate species. 

ReIp & GOLIKOV (1991) and REID ef al. (1991) have 
described some new species of Littorina from the north- 
western Pacific. They have found the form of the pallial 
oviduct to be a useful taxonomic character. We agree that 
the form of the oviduct can be useful and we agree with 
Reid that there is a close relationship among L. subro- 
tundata, L. “kurila,”’ and L. sp. and a more distant rela- 
tionship between these taxa and L. sitkana. What is less 
certain is whether it is advisable for REID & GOLIKOV 
(1991) to synonymize L. “kurila,’ L. sp., and L. subro- 
tundata into L. subrotundata, because they found no sig- 
nificant differences in the pallial oviduct or other anatom- 
ical characters. We think the fixed differences at the Pep-3 
locus for two populations of L. sp. and of L. subrotundata 
make it unlikely these two taxa are conspecific. While 
direct development can result in increased microgeographic 
differentiation within a taxon (e.g., JANSON & WARD, 1984), 
it may also promote speciation because of the reduced levels 
of gene flow (see BOULDING, 1990). 

The divergence between Littorina “kurila” and L. sitkana 
may have resulted as they moved south and encountered 
opposing selective pressures on exposed and protected shores 
(BOULDING, 1990a) and may have resulted in the exposed- 
shore species L. sp. Littorina sp. and L. “kurila” are thin- 
shelled and would be unlikely to persist where crabs were 
abundant (Boulding & Van Alstyne, unpublished data). 
No intertidal, shell-breaking crabs were observed on Adak 
Island where L. sitkana and L. “‘kurila” were collected (G. 
J. Vermeij, personal communication). In contrast, the thick 
shell of L. sitkhana makes it resistant to predation by shore 
crabs (Boulding & Van Alstyne, unpublished data; Beh- 
rens Yamada & Boulding, unpublished data) which are 
abundant on protected shores in the northeastern Pacific. 


ACKNOWLEDGMENTS 


We thank G. M. Davis, R. T. Dillon, Jr., D. Eernisse, 
T. Hay, K. Johannesson, P. Kemp, J. Kingsolver, D. G. 
Reid, and especially A. J. Kohn for comments on earlier 
versions of this manuscript; D. Eernisse, M. Kohn, and 
M. Strathmann for technical advice; H. Dang, T. Hay, 
C. Lundmark, Jj. Rosenthal, J. Slocum, K. Freeman, M. 
Li, K. Puckett, A. Sewell, and S. Stephens for technical 
assistance; and S. Behrens Yamada, R. C. Bullock, D. 
Duggins, C. McFadden, P. Marino, D. G. Reid, and G. 
Van Vliet for collecting snails. We are grateful to the 
directors and staff of Friday Harbor Laboratories, and the 
director and staff of Bamfield Marine Station. We thank 
the Makah Tribal Council and R. T. Paine for allowing 
us to work on Tatoosh Island. 

Financial assistance was provided by N.S.F. grant No. 
BSR-8700523 to A. J. Kohn, N.S.F. grant No. OCE- 
8415258 to R. R. Strathmann and D. J. Eernesse, N.S.F. 


The Veliger, Vol. 36, No. 1 


grant No. BSR-8715534 to R. R. Strathmann and P. J. 
Kemp, N.S.F. grant No. OCE-8614463 to R. T. Paine, 
a National Sciences and Engineering Research Council 
Canada operating grant to F.-S. Chia and by the following 
grants to E. G. Boulding: a National Sciences and Engi- 
neering Research Council Canada postgraduate scholar- 
ship and postdoctoral fellowship, a Sigma Xi grant-in-aid 
of research, the American Museum of Natural History’s 
Lerner Gray fund for marine research, two Pacific North- 
west Shell Club scholarships, and a Sarah DeLaney schol- 
arship from the Santa Barbara Shell Club. 


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The Veliger 36(1):69-71 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A New Ashmunella 
(Gastropoda: Pulmonata: Polygyridae) 


from Sonora, Mexico 


RICHARD L. REEDER 


Faculty of Biological Science, University of Tulsa, Tulsa, Oklahoma 74104, USA 


Abstract. 


A new species of Ashmunella is described from near Cananea in Sonora, Mexico, and 


comparisons are made with the closely related Chiricahuan species. 


INTRODUCTION 


This paper describing a new species of Ashmunella is part 
of a continuing study of the morphology and systematics 
of members of this genus. For comparative material I have 
relied heavily on the collection of Walter B. Miller as well 
as personal collections over the last 22 years. 


Ashmunella milesi Reeder, sp. nov. 
(Figures 1—5) 


Diagnosis: A medium-sized, depressed Ashmunella with a 
tridentate aperture and having an additional parietal cal- 
lous in about 50% of the individuals; with the upper cham- 
ber of the bipartite penis narrower and longer than the 
lower chamber; with relatively long epiphallus and short 
epiphallic caecum. 


Description of shell of holotype: Shell (Figures 1-3) of 
moderate size, depressed, lenticulate with relatively sharp 
shoulder and with open umbilicus, umbilicus contained 
about 6.0 times in the diameter of the shell. Color pale 
brown. Aperture with lip sharply reflexed, narrow, having 
two narrow basal teeth and a single, broader palatal tooth. 
Parietal wall with a prominent tooth and a smaller callous 
above the main tooth lying somewhat deeper within the 
aperture. Embryonic shell smooth with postembryonic 
whorls showing faint radially arranged bumps with nu- 
merous spirally arranged incised lines, the latter becoming 
prominent on the body whorl both above the periphery 
and on base of shell. Prominent radial growth ridges on 
all major whorls. 

Diameter 13.5 mm, height 6.2 mm, umbilicus 2.3 mm, 
number of whorls 6.5. 


Reproductive anatomy of holotype: The genitalia (Fig- 


ure 5) are typical of the genus, with a bipartite penis, a 
relatively long epiphallus, and a short epiphallic caecum. 
The penial retractor inserts on the epiphallus. The sper- 
matheca is long and tubular without a terminal enlarge- 
ment. Upper chamber of penis is about 2.5 times as long 
as the lower chamber from which it is sharply demarcated; 
lower chamber is considerably broader than the upper. 
Measurements of genital structures are as follows: 


lower penis 2.0 mm 
upper penis 5.4 mm 
epiphallus 14.0 mm 
epiphallic caecum 2.4 mm 
spermatheca 19.6 mm 


Variations in paratypes: A total of 39 adult shells was 
examined. These ranged in diameter from 12.1 mm to 13.6 
mm with an average of 12.85 mm. The height ranged from 
5.1 mm to 6.5 mm with an average of 5.95 mm. All of the 
unworn specimens exhibited the characteristic radial growth 
ridges and impressed spiral lines, and most exhibited elon- 
gate pustules (Figure 4). A total of 19 of the shells exhibited 
the extra parietal callous to some degree. 


Description of types: Holotype: Santa Barbara Museum 
of Natural History No. 35609. Paratypes: The Academy 
of Natural Sciences of Philadelphia No. 392397; U.S. Na- 
tional Museum No. 860573; collections of C. D. Miles, 
W. B. Miller, and R. L. Reeder. 


Type locality: Northern Sonora, Mexico, west of Cana- 
nea; south-facing talus slope along road to microwave tow- 
er, Sierra Mariquita; 31°2.0’N, 110°22.4’W; elevation ca. 
2000 m. Collected 17 May 1988 by S. J. McKee, W. B. 
Miller, and R. L. Reeder. 


Discussion: Species of Ashmunella were reviewed by 


Page 70 


The Veliger, Vol. 36, No. 1 


A ie 


25kV 2aGum 


x2aa Bead 


Explanation of Figures 1 to 4 


Figures 1-3. Ashmunella milesi sp. nov. Shell of holotype SBMNH 35609; diameter 13.5 mm. Aperture, apical, 
and umbilical views respectively. Figure 4. SEM view of typical sculpture (paratype). 


PILsBRY (1940) with additional comments provided by 
BEQUAERT & MILLER (1973) and MILLER (1983). Ash- 
munella milest is clearly related to the Chiricahuan species 
of Arizona as indicated by the narrow upper penis shared 
with those species. It differs from all of those species, 
however, in that the upper division of the penis is consis- 
tently longer. In the specimens dissected, the upper penis 
is 2.5 times or more the length of the lower portion. No 
species in the Chiricahuan group has an upper penis great- 
er than 1.5 times that of the lower division. 

The shell of Ashmunella milesi resembles most closely 
that of Ashmunella lenticula Gregg (see GREGG, 1953). Both 
species are similar in overall size, the size of the umbilicus, 
and the sharpness of the shoulder. The parietal tooth is 
sinuous in A. lenticula and relatively straight in A. milesz. 
The extraparietal callous present in many specimens of A. 
milesi is never present in A. lenticula. 


Distribution and habitat: Ashmunella milesi is known 
only from the type locality, although thorough exploration 


of the Sierra Mariquita is incomplete. Vegetation at the 
type locality consists principally of Rhus trilobata, Yucca 
shotti, Juniperus deppeana, Quercus arizonica, Quercus ob- 
longifolia, Quercus emoryi, and Pinus cembroides. 


Etymology: This species is named for Dr. Charles D. 
Miles, who first introduced me to the study of land snails 
and sent me off to study them in my beloved desert. 


ACKNOWLEDGMENTS 


I wish to thank Susan J. McKee for companionship in the 
field and for preparation of the drawings and photographs. 
Thanks also to Walt Miller for companionship in the field, 
the loan of specimens, and reading the manuscript. Jim 
Hoffman was also kind enough to read the paper. My 
students Wendy Shaffer and Michael Kalcich helped in 
the lab, and finally thanks to Dr. Al Soltow and the re- 
search office of the University of Tulsa, who kindly fi- 
nanced some of the field work and materials for this study. 


Resa weeder 993 


Page 71 


10 mm 


Figure 5 


Anterior portion of reproductive system of holotype of Ashmunella 
milest sp. nov. Drawing prepared from projection of stained 
wholemount, RLR 813A (SBMNH 35609). Key: ag, albumin 
gland; ep, epiphallus: epc, epiphallic caecum; Ip, lower penis; pt, 
prostate; sp, spermatheca; up, upper penis; ut, uterus; va, vagina; 
vd, vas deferens. Arrows indicate limits of upper penis. 


LITERATURE CITED 


BEQUAERT, J. C. & W. B. MILLER. 1973. The Mollusks of 
the Arid Southwest with an Arizona Check List. University 
of Arizona Press: Tucson, Arizona. i-xvi, 271 pp.; 7 figs. 

GreGG, W. O. 1953. Two new land snails from Arizona. 
Bulletin of the Southern California Academy of Science 52(2): 
71-75. 

MILLER, W. B. 1983. Ashmunella angulata Pilsbry, 1905, Ash- 
munella esuritor Pilsbry, 1905, Ashmunella lenticula Gregg, 
1953, Ashmunella lepiderma Pilsbry & Ferriss, 1910 and 
Ashmunella varicifera (Ancey, 1901) re-established as valid 
species. The Veliger 25(3):266. 

Piusspry, H. A. 1940. Land Mollusca of North America (North 
of Mexico). Academy of Natural Sciences, Philadelphia, 
Monograph No. 3, 1(2):i—vili, 575-994, i-ix. 


The Veliger 36(1):72-77 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


First Oligocene Records of Calyptogena 


(Bivalvia: Vesicomyidae) 


JAMES L. GOEDERT 


15207 84th Ave. Ct. NW, Gig Harbor, Washington 98329, and 
Museum Associate, Section of Vertebrate Paleontology, Natural History Museum of Los Angeles County, 
900 Exposition Boulevard, Los Angeles, California 90007, USA 


RICHARD L. SQUIRES 


Department of Geological Sciences, California State University, Northridge, California 91330, USA 


Abstract. 


Fossils of the vesicomyid bivalve Calyptogena (Calyptogena) chinookensis Squires & Goedert, 


1991, from probable subduction-related localized limestones in the Lincoln Creek and Pysht formations, 
and turbidity-flow deposits in middle part of the Makah Formation in western Washington, are the 
first unequivocal Oligocene records for the genus. Previously, C. (C.) chinookensis was known only from 
late middle to late Eocene subduction-related cold-methane-seep communities in limestones in south- 
western Washington. The geologic range of C. (C.) chinookensis is now extended from late middle Eocene 
to late Oligocene. ‘The hinge dentition of this species is observed for the first time and compares well 


with that of the subgenus Calyptogena. 


INTRODUCTION 


The vesicomyid bivalve genus Calyptogena includes mod- 
ern species that can be members of deep-sea chemosyn- 
thesis-dependent communities near hydrothermal vents 
(Boss & TURNER, 1980), subduction-zone related cold- 
seeps (OHTA & LAUBIER, 1987), hydrocarbon seeps 
(KENNICUTT ef al., 1985; CALLENDER et al., 1990), and 
even decaying whale carcasses (SMITH ef al., 1989). The 
fossil record of Calyptogena extends from late middle Eo- 
cene to Recent (GOEDERT & SQUIRES, 1990; SQUIRES & 
GOEDERT, 1991). Ancient examples of chemosynthetic 
communities containing Calyptogena are rare and so far 
have been confined to subduction-related communities in 
Miocene and Pliocene deposits in Japan (KANNO et al., 
1989; NuTSsUMA et al., 1989) and late middle to late Eocene 
limestones in southwestern Washington (GOEDERT & 
SQUIRES, 1990; SQuIRES & GOEDERT, 1991). These de- 
posits in Washington contain Calyptogena (C.) chinookensis 
Squires & Goedert, 1991, which is the earliest known 
species of the genus. 

Recent field work indicates that Calyptogena (C.) chi- 
nookensis 1s present sporadically throughout the Paleogene 


deep-marine sediments in western Washington State (Fig- 
ures 1, 2). Newly collected specimens (Figures 3-5) from 
several Oligocene formations in western Washington allow 
for a geologic range extension of this species into the late 
Oligocene and also allow, for the first time, a description 
of the hinge. Some of the new material is associated with 
localized limestones that apparently were derived in as- 
sociation with subduction-zone processes. The presence of 
C. (C.) chinookensis in these formations represents the first 
unequivocal Oligocene occurrences of the genus Calypto- 
gena. Previously, Boss & TURNER (1980:163-164) had 
tenuously reported Calyptogena as ranging from Oligocene 
to Recent. 

The institutional abbreviation, LACMIP = Natural 
History Museum of Los Angeles County, Invertebrate 
Paleontology Section, Los Angeles, California, is used for 
locality and catalog numbers. 


MATERIALS anD METHODS 


Specimens of Calyptogena (C.) chinookensis were collected 
from blocks of weathered limestone in the upper part of 
the Lincoln Creek Formation at locality LACMIP 5843 


J. L. Goedert & R. L. Squires, 1993 


Page 73 


Figure 1 


Index map of western Washington State showing new collecting 
localities for Calyptogena (C.) chinookensis. 


near the townsite of Knappton, Washington (Figure 1). 
This locality is one of several along the north shore of the 
Columbia River that have together yielded a diverse and 
well studied fossil invertebrate fauna (ZULLO, 1982; RIGBY 
& JENKINS, 1983; MooreE, 1984a, b; SQUIRES, 1989). The 
presence of C. (C.) chinookensis in this fauna was not 
previously noticed. 

At locality LACMIP 5843, most collections of fossils 
are usually from abundant concretions that have eroded 
from mudstone exposed on the beach terrace and in modern 
landslides (MooreE, 1984b). The concretions range in size 
from a few millimeters to more than 1 m in diameter, and 
most are barren of fossils. The specimens of Calyptogena 
(C.) chinookensis were found in blocks of micritic limestone 
that have been transported downslope in landslides and 
are now mixed with the more abundant concretions. The 
limestone blocks are up to 1 m long and differ from the 
concretions in being more angular and lighter in color. 
The limestone blocks also have a strong petroliferous odor 
when freshly broken, and they contain thin-to-thick wavy 
crusts of calcite and numerous small tubes or cavities lined 
with calcite or quartz crystals. The limestone is locally 
brecciated and usually bioturbated. Where the limestone 
contains fossils, they are usually articulated specimens of 
the bivalves C. (C.) chinookensis (up to 33 mm length), 


OLYMPIC 
PENINSULA 


SOUTHWEST 
WASHINGTON 


PYSHT FM. 
* LACMIP 5843 


LINCOLN 
CREEK FM. 


* LACMIP 15621 


= LACMIP 6295 


z 
=< 
o 
oc 
O 
= 
Lu 
N 


MAKAH FM. 


Figure 2 


Time-stratigraphic chart showing previous range (slanted lines) 
of Calyptogena (C.) chinookensis and position of new localities for 
this species. Data in part from ARMENTROUT et al. (1983). JC 
= Jansen Creek Member of the Makah Formation; SCP = 
“Siltstone at Cliff Point” of WELLS (1989). 


Thyasira sp. (up to 40 mm length), and Modiolus willa- 
paensis Squires & Goedert, 1991 (up to 30 mm length). 
In addition to these, the limestone also contains rare spec- 
imens of the bivalve Acharax sp., venerid(?) bivalves, small 
gastropods, and wood fragments. Some of the thyasirids 
are hollow and lined with calcite or quartz crystals. A few 
of the specimens of Calyptogena are partially silicified, and 
a fragment of the right-valve hinge (Figure 4) was recov- 
ered by etching with dilute formic acid. 

Specimens of Calyptogena (C.) chinookensis were also 
found at localities LACMIP 6295 and LACMIP 15621 
in the lower part of the Pysht Formation west of the mouth 
of Murdock Creek, Clallam County, Washington (Figure 
1). Invertebrate macrofossils from these rocks were studied 


Page 74 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 3 and 4 


Figures 3, 4. Calyptogena (C.) chinookensis Squires & Goedert, 1991. Figure 3. Left-valve hinge, x6, hypotype 
LACMIP 12099, locality LACMIP 15622. Figure 4. Right-valve hinge, x8.9, hypotype LACMIP 12097, locality 


LACMIP 5843. 


by DURHAM (1944), but he did not note the presence of 
Calyptogena. At these localities, concretions are abundant 
as lag materials eroded from beach cliffs and the beach 
terrace along the south shore of the Strait of Juan de Fuca. 
Mixed with the concretions are blocks of micritic limestone 
up to | m across. This limestone is almost identical to that 
from the Lincoln Creek Formation at Knappton (LAC- 
MIP 5843). 

Where the limestone at localities LACMIP 6295 and 
LACMIP 15621 contain fossils, they are articulated spec- 
imens of the bivalves Calyptogena (C.) chinookensis (from 
5.5 to 25 mm length), 7hyasira sp. (up to 33 mm length), 
and Modiolus willapaensis? (up to 42 mm length). In ad- 
dition, the limestone may contain a few pogonophoran(?) 
tubes, minute gastropods, spatangoid echinoids, crinoid 
UIsocrinus?) parts, and rare wood fragments. Some of the 
bivalves are hollow and lined with quartz crystals. This 
limestone has not yet been seen 77 situ at locality LACMIP 
6295 or LACMIP 15621, but field observations suggest 
that the source rock is the same as that producing the 
abundant concretions. 

A few specimens of Calyptogena (C.) chinookensis were 
collected from approximately the middle part of the Makah 
Formation at locality LACMIP 15622, southeast of the 
mouth of Bullman Creek, Clallam County, Washington 
(Figure 1). This locality is in the toe of a modern landslide 
that largely consists of dark-colored mudstone beds with 
thin slabs of turbidite sandstone and conglomerate most 
likely from stratigraphically below the Jansen Creek 
Member of the Makah Formation. The Jansen Creek 
Member, which is situated in the middle part of the Makah 
Formation, is exposed on the beach terrace in all directions 
from the toe of the landslide. Some of the slabs of thin 
turbidites eroding from the landslide consist of graded 
sandstone to pebble conglomerate containing glauconite, 
foraminifera, some mollusk fragments, rare shark teeth, 
fish otoliths, and usually articulated specimens of C. (C.) 
chinookensis (22 to 42 mm length) and Thyasira sp. (up to 
40 mm length). The bivalves are usually together in clus- 
ters of several randomly oriented individuals in fine-grained 


sediment between larger clasts (up to 9.5 cm across) of 
siltstone (reworked concretions?) and sandstone. The bi- 
valves do not appear to have been transported, but they 
have been slightly crushed by sediment compaction. One 
specimen of C. (C.) chinookensis was prepared to reveal 
the left-valve hinge (Figure 3). 


DEPOSITIONAL ENVIRONMENTS AnpD 
GEOLOGIC AGES 


Molluscan fossils from the upper part of the Lincoln Creek 
Formation near Knappton, including locality LACMIP 
5843, suggest that deposition took place at depths between 
100 and 350 m; however, foraminifers indicate a depth of 
1000 m or possibly deeper (Moore, 1984b:7-8). Mollus- 
can fossils referable to the Juanian Molluscan Stage, along 
with microfossils, indicate a late Oligocene to earliest Mio- 
cene age (Moore, 1984a, b). 

Foraminifera from rocks in the vicinity of localities 
LACMIP 6295 and LACMIP 15621 indicate that de- 
position probably occurred at a depth of between 300 and 
2000 m during late Oligocene (Zemmorian) time (RAU, 
1964). Localities LACMIP 6295 and LACMIP 15621 
are both within DURHAM’s (1944) Echinophoria rex Mol- 
luscan Zone in the lower part of the ““T'win Rivers For- 


Figure 5 


Calyptogena (C.) chinookensis Squires & Goedert, 1991. Left-valve 
exterior, 3.9, hypotype LACMIP 12098, locality LACMIP 
15621. 


J. L. Goedert & R. L. Squires, 1993 


mation” (now Pysht Formation of the Twin River Group, 
see SNAVELY et al., 1977). The Echinophoria rex (now 
Liracassis rex) Molluscan Zone is correlative with the Mat- 
lockian Molluscan Stage and the lower Zemmorian Fo- 
raminiferal Stage, which is early Oligocene in age (MOORE, 
1984a). DURHAM (1944) considered these rocks to be mid- 
dle Oligocene, and DOMNING et al. (1986:7) stated that 
these rocks are middle or late, but not latest, Oligocene in 
age. The zonal gastropod Liracassis apta (Tegland, 1931) 
has also been collected from this part of the Pysht For- 
mation (GOEDERT, 1988:100). The L. apta Molluscan Zone 
is correlative with the Juanian Molluscan Stage, the upper 
part of the Zemmorian Foraminiferal Stage, and is late 
Oligocene to earliest Miocene in age (Moore, 1984a). 
The age of the entire Pysht Formation is shown as late 
Oligocene and earliest Miocene by ARMENTROUT ef al. 
(1983). Because both L. rex and L. apta are present in the 
lower part of the Pysht Formation west of Murdock Creek, 
this part of the formation is herein considered temporally 
equivalent to the upper part of the Makah Formation 
(Figure 2). 

The co-occurrence of Calyptogena (C.) chinookensis in 
essentially identical limestones at localities LACMIP 5843, 
LACMIP 6295, and LACMIP 15621, along with the 
same associations of thyasirid and modiolid species, are 
much like those previously described from Eocene deep- 
water strata in western Washington by GOEDERT & 
SQUIRES (1990) and SQUIRES & GOEDERT (1991). Those 
Eocene associations were interpreted as fossil cold-meth- 
ane-seep communities, and the associations from localities 
LACMIP 5843, LACMIP 6295, and LACMIP 15621 
may have also been chemosynthesis-dependent commu- 
nities supported by cool-fluid seepage. 

The occurrence of Calyptogena (C.) chinookensis at lo- 
cality LACMIP 15622, with associated thyasirids in tur- 
bidites of the Makah Formation (Figure 2), is the first in 
which the species is not in a limestone. Calyptogena has 
been reported living in association with thyasirids in mod- 
ern turbidity flow deposits (MAYER et al., 1988), and rocks 
at locality LACMIP 15622 may represent a similar de- 
positional environment. Rocks of the Makah Formation 
were rapidly deposited in a submarine-fan setting at lower 
to middle bathyal depths, and are late Eocene to Oligocene 
in age (SNAVELY et al., 1980). The rocks containing the 
specimens of C’ (C.) chinookensis are from below the Jansen 
Creek Member and are early Oligocene in age. Macro- 
fossils are rare in these deep-water strata, although a few 
thyasirid, modiolid, and lucinid bivalves have been found 
associated with fossil cetacean skeletons (SQUIRES et al., 
1991). These associations were the first known fossil ex- 
amples of chemosynthesis-dependent organisms supported 
by whale bone-oil seepage. 


SYSTEMATIC PALEONTOLOGY 
Family VESICOMYIDAE Dall & Simpson, 1901 


Genus Calyptogena Dall, 1891 


Page 75 


Type species: Calyptogena pacifica Dall, 1891 


Subgenus Calyptogena s.s. 


Calyptogena (Calyptogena) chinookensis 
Squires & Goedert, 1991 


(Figures 3—5) 


Supplementary description: Right-valve hinge—anteri- 
or tooth solid, peglike, and directed posteriorly; central 
tooth triangular and prolonged anteriorly into a very thin 
plate that overlaps dorsal part of anterior tooth; posterior 
tooth area unknown. Left-valve hinge—apparently no an- 
terior tooth; central tooth bifid with a solid posterior part 
and a thin anterior part; posterior tooth area unknown. 


Discussion: The hinge of this species closely resembles 
that of Calyptogena (C.) pacifica Dall, 1891, illustrated by 
BERNARD (1974:text fig. 2A) and Boss & TURNER (1980: 
fig. 10b). Because of this close similarity, it is herein con- 
cluded that C. chinookensis should be assigned to the sub- 
genus Calyptogena. 

Boss & TURNER (1980) suggested that Calyptogena 
ranged from as early as Oligocene time on the basis of the 
tenuous inclusion of the genera Pleurophopsis Van Winkle, 
1919, and Hubertschenckia Vakeda, 1953, in their syn- 
onymy of Calyptogena. Pleurophopsis is known from Oli- 
gocene(?) rocks of the West Indies, Central America, and 
northwestern South America (KEEN, 1969). The close re- 
lationship between Calyptogena and Pleurophopsis unioides 
VAN WINKLE (1919:24, pl. 3, fig. 12), the type species of 
Pleurophopsis, was first noted by WOODRING (1938). The 
geologic age of P. unioides remains in question, and it may 
be as young as Pliocene (Boss & TURNER, 1980:164). 

OLsson (1931) reported two species of Pleurophopsis 
from probable late Oligocene-age rocks in northern Peru. 
One of these, P. lithophagoides OLSSON (1931:140, pl. 4, 
figs. 2, 5, 7, 9) shows close affinity with Calyptogena (C.) 
chinookensis. Calyptogena (C.) chinookensis differs in having 
the following features: larger size (up to 100 mm length 
rather than 40 mm), presence of a narrow ridge postero- 
ventrally from the umbo, and posterior end more tapered. 

Boss & TURNER (1980) mentioned a possible Oligocene 
occurrence of Pleurophopsis from Colombia. The hinge 
structure is unknown for this specimen(s), and no strati- 
graphic information was given. As mentioned by OLSSON 
(1931), Unio bitumen COOKE (1919:130, pl. 9, fig. 3a—c) 
from presumed Oligocene-age rocks in Cuba probably also 
is congeneric with Pleurophopsis. The hinge structure is 
also unknown for this species, and stratigraphic infor- 
mation is limited. 

Hubertschenckia Takeda, 1953, is known from late Oli- 
gocene rocks in Japan (TAKEDA, 1953; KEEN, 1969). The 
close relationship between Calyptogena and Hubertschenck- 
ia was first suggested by KANNO (1971). Future work may 
prove that these two genera are the same, but H. ezoensis 
(YOKOYAMA, 1890:pl. 25, figs. 6a, b, 7, 8), the type species 


Page 76 


of Hubertschenckia, has a shell that is much higher relative 
to length than do most species of Calyptogena. 

As indicated by Boss & TURNER (1980), it is quite likely 
that Pleurophopsis and Hubertschenkia are actually syn- 
onyms for Calyptogena. If so, then Calyptogena is tenuously 
known from Oligocene rocks in the West Indies, Central 
America, northwestern South America, and Japan. The 
occurrences of C. (C.) chinookensis in the upper part of the 
Lincoln Creek, lower part of the Pysht, and middle part 
of the Makah formations in Washington are the first un- 
equivocal Oligocene records for this genus and the first 
report of it in the Oligocene in North America. 


ACKNOWLEDGMENTS 


We thank Louie Marincovich, Jr. (U.S. Geological Sur- 
vey, Menlo Park, California) for providing a copy of the 
hard-to-obtain reference by TAKEDA (1953). Field work 
that resulted in the discovery of Calyptogena in the Pysht 
and Makah formations was supported by a grant (4439- 
90) from the National Geographic Society. Gail H. Goe- 
dert assisted with field work. We thank Ellen J. Moore 
and an anonymous reviewer for comments on the manu- 
script. 


LOCALITIES CITED 


LACMIP 5843. Float on beach terrace, from landslides, 
N shore of the Columbia River, in NE part of the 
bay between Grays Point and Knappton, approxi- 
mately 305 m S and 430 m E of the NW corner of 
section 9, TON, ROW, Knappton quadrangle (USGS), 
7.5 minute, 1949 (photorevised 1973), Pacific County, 
Washington. Upper part of Lincoln Creek Formation. 
Age: Late Oligocene. Collectors: J. L. & G. H. Goe- 
dert, 26 January 1992. 

LACMIP 6295. Float on beach terrace between 300 m 
and 850 m W of the mouth of Murdock Creek, NW 
section 29, T31N, ROW, Disque quadrangle (USGS), 
7.5 minute, 1950 (photorevised 1978), Clallam Coun- 
ty, Washington. Lower part of Pysht Formation. Age: 
Early(?) Oligocene. Collectors: J. L. & G. H. Goe- 
dert, 31 May 1992. 

LACMIP 15621. Limestone blocks on beach terrace, S 
shore of Strait of Juan de Fuca, approximately 1500 
m NW of the mouth of Murdock Creek, 450 m W 
and 200 m N of the SE corner of section 19, T31N, 
ROW, Twin Rivers quadrangle (USGS), 7.5 minute, 
1950 (photorevised 1979), Clallam County, Wash- 
ington. Lower part of Pysht Formation. Age: Early(?) 
Oligocene. Collectors: J. L. & G. H. Goedert, 23 
March 1992. 

LACMIP 15622. Thin slabs of turbidite sandstone and 
pebble conglomerate in dark mudstone in toe of a 
landslide, approximately 2050 m SE of the mouth of 
Bullman Creek, NW% SW'% section 22, T33N, 
R14W, Neah Bay quadrangle (USGS), 7.5 minute, 


The Veliger, Vol. 36, No. 1 


prov. ed. 1984, Clallam County, Washington. Ap- 
proximately middle part of Makah Formation (di- 
rectly below the Jansen Creek Member). Age: Early 
Oligocene. Collector: J. L. Goedert, 18 May 1992. 


LITERATURE CITED 


ARMENTROUT, J. M., D. A. HuLL, J. D. BEAULIEU & W. W. 
Rau. 1983. Correlation of Cenozoic stratigraphic units of 
western Oregon and Washington. Oregon Department of 
Geology and Mineral Industries, Oil and Gas Investigations 
7:1-90. 

BERNARD, F. R. 1974. The genus Calyptogena in British Co- 
lumbia with a description of a new species (Bivalvia, Ves- 
icomyidae). Venus 33:11-22. 

Boss, K. J. & R. D. TURNER. 1980. The giant white clam 
from the Galapagos Rift, Calyptogena magnifica species no- 
vum. Malacologia 20:161-194. 

CALLENDER, W. R., G. M. STAFF, E. N. POWELL & I. R. 
MacDona.p. 1990. Gulf of Mexico hydrocarbon seep 
communities. V. Biofacies and shell orientation of autoch- 
thonous shell beds below storm wave base. Palaios 5:2-14. 

Cooke, C. W. 1919. Tertiary mollusks from the Leeward 
Islands and Cuba. Carnegie Institution of Washington Pub- 
lication 291:103-156. 

DALL, W. H. 1891. On some new or interesting west American 
shells obtained from the dredgings of the U.S. Fish Com- 
mission steamer Albatross in 1888, and from other sources. 
United States National Museum, Proceedings 14:173-191. 

DALL, W. H. & C. T. Stwpson. 1901. The Mollusca of Porto 
Rico. United States Fisheries Commission, Bulletin 20:351- 
524. 

DoMNING, D. P., C. E. Ray & M. C. McKENNA. 1986. Two 
new Oligocene desmostylians and a discussion of Tethytheri- 
an systematics. Smithsonian Contributions to Paleobiology 
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The Veliger 36(1):78-80 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A New Muricopsis from the Gulf of 


California, Mexico 


BARBARA W. MYERS anD CAROLE M. HERTZ 


Associates, Department of Marine Invertebrates, San Diego Natural History Museum, 
Balboa Park, P.O. Box 1390, San Diego, California 92112, USA 


ANTHONY D’ATTILIO 


2415 29th Street, San Diego, California 92104, USA 


Abstract. 


A new species of Muricopsis collected at Isla Danzante, Gulf of California, Mexico, is 


described. Originally confused with Nipponotrophon galapaganus (Emerson & D’Attilio, 1970), the new 
species is compared with two closely related congeners, Muricopsis armatus (A. Adams, 1854) and M. 


jaliscoensis Radwin & D’Attilio, 1970. 


INTRODUCTION 


SKOGLUND (1983:108) figured this new species as Nip- 
ponotrophon galapaganus (Emerson & D’Attilio, 1970) from 
off Isla Danzante, Gulf of California, Mexico (25°45'N, 
111°15’'W). VoKEs (1988:33) rejected this identification 
and indicated that the specimen figured by Skoglund was 
probably a new species of Muricopsis. Those identifications 
were based on a dead specimen lacking protoconch and 
operculum. In 1989 two living specimens were dredged by 
Skoglund, and another living specimen was dredged by 
Hertz and Skoglund in 1991, all at the original location. 
Our examination of these specimens, including the pro- 
toconch, the radula, and the operculum, confirmed that 
they are not Nipponotrophon galapaganus but, indeed, are 
a new species of Muricopsis. 

Institutional abbreviations are as follows: AMNH, 
American Museum of Natural History, New York; LACM, 
Natural History Museum of Los Angeles County; 
SBMNH, Santa Barbara Museum of Natural History; 
and SDNHM, San Diego Museum of Natural History. 


SYSTEMATICS 
MURICIDAE Rafinesque, 1815 
MURICOPSINAE Radwin & D’Attilio, 1971 
Muricopsis Bucquoy & Dautzenberg, 1882 


Type species: Murex blainviller Payraudeau, 1826, by orig- 
inal designation 


Muricopsis skoglundae 
Myers, Hertz & D’Attilio, sp. nov. 


(Figures 1-5) 


Description: Holotype fusiform; spire high, acute; pro- 
toconch eroded (Figures 1, 2). Paratype with a protoconch 
of 1% unsculptured, brown, rounded whorls (Figure 3). 
Suture weakly defined; eight teleoconch whorls; aperture 
ovate with shallow anal sulcus directed towards columella; 
outer lip erect, crenulate, reflecting external sculpture, six 
denticles within, all but most posterior prominent; colu- 
mellar lip adherent at sulcus, detached and erect below; 
siphonal canal long, open, recurved. Six varices, crossing 
shoulder to suture. Four major spiral cords, three on body 
whorl, one on canal, terminating at each varix in long, 
recurved, open lamellose spines; minor cords with small 
lamellose spines between major spines. Canal with gap at 
juncture of body whorl. Operculum corneous, unguiculate 
with basal nucleus (Figure 4). Color cream to light tan 
with single, indistinct brown band on body whorl between 
second and third major cords. Spines suffused with pale 
rose; aperture white. Radula with central rachidian tooth 
and single lateral on each side; rachidian with five cusps, 
a strong central, two laterals, two minor intermediate cusps, 
and strong single endpoints (Figure 5). 


B. W. Myers et al., 1993 


Page 79 


Explanation of Figures 1 and 2 


Figures 1, 2. Muricopsis skoglundae sp. nov. Holotype, SBMNH 35610. Height 45.8 mm, width 28.0 mm. Off 
south end of Isla Danzante, Gulf of California, Mexico, in 30-45 m. Figure 1. Apertural view. Figure 2. Dorsal 


view. 


Etymology: It gives us great pleasure to name the species 
in honor of Carol Skoglund of Phoenix, Arizona, who 
collected the first three specimens and has been convinced 
since 1981 that it was a new species. 


Type locality: Just south of Isla Danzante, Gulf of Cal- 
ifornia, Mexico (25°45'N, 111°15’W) in 30-45 m. 


Type material: Three specimens from type locality dredged 
by Carol and Paul Skoglund, October 1981 and October 
1989. Holotype: SBMNH 35610, 45.8 mm long, 28.0 mm 
wide. Paratypes: AMNH 232521, one specimen 38.3 mm 
long, 24.8 mm wide; one paratype retained in the Carol 
Skoglund collection, 26.7 mm long and 21.6 mm wide. 
One paratype, 48.4 mm long and 27.4 mm wide, dredged 
by Hertz and Skoglund, October 1991, at type locality, on 
upper valve of Hyotissa hyotis (Linnaeus, 1758), retained 
in Hertz collection. 


Remarks: The AMNH paratype, a dead-collected spec- 
imen, is the specimen identified as Nipponotrophon gala- 
paganus (Emerson & D’ Attilio, 1970) in SKOGLUND (1983). 
The paratype in the Skoglund collection, a young live- 
collected specimen with protoconch and immature lip, is 
tan to light brown with pink spines. The Hertz collection 


paratype is a mature, live-collected specimen, with a white 
to cream shell with a pale rose blush on the long spines. 


Discussion: Muricopsis skoglundae is compared here with 
specimens of M. armatus in the SDNHM and Skoglund 
collections, the types of M. jaliscoensis (holotype SDNHM 
51251; paratypes SONHM 51250, 51015, 51285) and, 
for clarity, Nipponotrophon galapaganus (holotype AMNH 
155906; paratypes AMNH 155907, LACM 1233) anda 
paratype in the Donald R. Shasky collection. 

Muricopsis skoglundae has 142 unsculptured rounded 
nuclear whorls. In contrast, M. armatus, its closest con- 
gener, has 12 sharply angulate nuclear whorls with shoul- 
der and median cords (MYERS & D’ATTILIO, 1986:71). 
Although both species have a similar fusiform shape, M. 
skoglundae has only six varices and three major cords on 
the body whorl, whereas M. armatus has seven varices and 
four major cords on the body whorl. The spines formed 
where cords and varices intersect are long, recurved and 
widely open in M. skoglundae, compared to M. armatus, 
which has straight, closed or narrowly open spines. There 
is a prominent knoblike denticle on the columella just above 
the siphonal canal in M. armatus, which is not found in 
the new species. The prominent gap in spiral sculpture 


Page 80 


The Veliger, Vol. 36, No. 1 


Explanation of Figures 3 to 5 


Figures 3-5. Muricopsis skoglundae sp. nov. Figure 3. Paratype, 
Skoglund collection. Height 26.7 mm, width 21.6 mm. Camera 
lucida drawing of protoconch. Figure 4. Holotype. Camera lucida 
drawing of radula. Figure 5. Holotype. Camera lucida drawing 
of exterior of operculum showing basal nucleus. 


between body whorl and canal, and the brown band on 
the body whorl] noted for M. skoglundae, are not apparent 
in M. armatus, which has uninterrupted major cords on 
the body whorl and siphonal canal and no brown band. 
Muricopsis skoglundae is quite different from M. jalisco- 
ensis, known from Jalisco and Colima in the Gulf of Cal- 
ifornia (RADWIN & D’ATTILIO, 1976) and Panama 
(D’ATTILIO, 1980:fig. 3 [fig. 1 and 4 should read M. ar- 
matus |). The shell of M. skoglundae is much larger, cream 
in color, possessing six varices with long spines and few 
spiral cords, whereas the holotype of M. jaliscoensis is 
brown, half the size of M. skoglundae, and has five varices 
with scabrous spiral cords over the entire surface and short 
spines. Muricopsis skoglundae, with a protoconch of 1% 
rounded, unsculptured whorls, has six denticles on the 
apertural lip and none on the columella, whereas M. jalis- 


coensis has a two-whorled tabulate protoconch and seven 
denticles on the apertural lip and three on the columella. 

Muricopsis skoglundae has 142 brown nuclear whorls, 
whereas Nipponotrophon galapaganus, known only from 
the Islas Galapagos, has 2 white nuclear whorls. The 
operculum of Muricopsis skoglundae has a basal nucleus, 
whereas in Nipponotrophon galapaganus the nucleus is sit- 
uated sublaterally (EMERSON & D’ATTILIO, 1970:fig. 4). 
Muricopsis skoglundae has scabrous sculpture and no in- 
tritacalx. In contrast, Nipponotrophon galapaganus has a 
smooth shell covered by a thick white intritacalx. The shell 
of Muricopsis skoglundae has strong varical spines which 
continue on the siphonal canal; Nipponotrophon galapa- 
ganus has no spines on the siphonal canal. 


ACKNOWLEDGMENTS 


We are grateful to William K. Emerson of the American 
Museum of Natural History, James H. McLean and 
Lindsey Groves of the Natural History Museum of Los 
Angeles County, and Donald R. Shasky of Redlands, Cal- 
ifornia, for the loan of type material. The San Diego Nat- 
ural History Museum made its facilities available to us 
and Regina Wetzer, Collections Manager, Department of 
Marine Invertebrates, kindly assisted in the mounting of 
the minute radula of Muricopsis skoglundae. We are in- 
debted to David K. Mulliner, who photographed the ho- 
lotype of the new species. William K. Emerson, James H. 
McLean, Walter E. Sage III, and Emily H. Vokes kindly 
reviewed the manuscript. Finally, Carol Skoglund is es- 
pecially thanked for giving us the opportunity to describe 
this beautiful new species. 


LITERATURE CITED 


ADAMS, A. 1854. Description of new shells from the collection 
of H. Cuming Esq. Proceedings of the Zoological Society of 
London 21:69-74 (1853). 

D’ATTILIO, A. 1980. Muricopsis jaliscoensis Radwin & D?’At- 
tilio, 1970 at Panama. The Festivus 12(6):78-79 (June). 

EMERSON, W. K. & A. D’ATTILIO. 1970. Three new species 
of muricacean gastropods from the eastern Pacific. The Ve- 
liger 12(3):270-273 (January 1). 

Myers, B. W. & A. D’ATTILIO. 1986. Comments on the pro- 
toconch in the Muricidae with illustrations. The Festivus 
18(5):55-77 (May 8). 

RapwIn, G. E. & A. D’ATTILIO. 1970. A new species of Mun- 
copsis from west Mexico. The Veliger 12(3):351-356 (Jan- 
uary 1). 

Rapwin, G. E. & A. D’ATTILIO. 1976. Murex Shells of the 
World; an Illustrated Guide to the Muricidae. Stanford Uni- 
versity Press: Stanford, California. 284 pp. 

SKOGLUND, C. 1983. Range extensions of Muricidae in the 
Gulf of California, Mexico. The Festivus 15(11):107-108 
(November 10). 

VoKEs, E. H. 1988. Muricidae (Mollusca: Gastropoda) of the 
Esmeraldas Beds, northwest Ecuador. Tulane Studies in 
Geology and Paleontology 21(1):1-58 (July). 


The Veliger 36(1):81-87 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


First Report of the Ovulid Gastropod 
Sulcocypraea mathewsonu (Gabb, 1869) from the 


Eocene of Washington and Oregon and an 


Additional Report from California 


by 


RICHARD L. SQUIRES 


Department of Geological Sciences, California State University, Northridge, California 91330, USA 


AND 


LINDSEY T. GROVES 


Malacology Section, Natural History Museum of Los Angeles County, 
900 Exposition Boulevard, Los Angeles, California 90007, USA 


Abstract. 


The warm-water ovulid gastropod Sulcocypraea mathewsonu (Gabb, 1869), previously 


known only from middle Eocene strata in southern and central California, is reported for the first time 
from middle Eocene strata in western Washington, as well as from an additional locality in southern 
California. The species is tentatively reported from middle Eocene strata in northwestern and south- 
western Oregon. The Washington locality is the northernmost record of any ovulid, fossil or living, in 
the eastern Pacific, and extends the geographic range of this species northward 1100 km. The geologic 
range of Sulcocypraea is restricted to the earliest Eocene to early Oligocene. 


INTRODUCTION 


Sulcocypraea (family Ovulidae) is an uncommon Paleogene 
gastropod genus known only from seven species in North 
America, one species in northern Peru, and one species in 
southwestern France. We report here new geographic rec- 
ords for the genus from midd!e Eocene strata in western 
Washington and southern California, and tentatively from 
middle Eocene strata in northwestern and southwestern 
Oregon. The Washington record, from a locality just south 
of Seattle (47°30'N latitude) is the northernmost for any 
ovulid, fossil or living, in the eastern Pacific. 

Ovulid gastropods live today in tropical to subtropical 
seas (ROSENBERG, 1992), and the presence of Sulcocypraea 
in Washington and Oregon indicates similar conditions. 
This would be in keeping with what has been reported 
for the paleoclimate of this area during the middle Eocene. 
On the basis of reef-coral genera and numerous genera of 
mollusks whose species today are particularly character- 
istic of warm waters, DURHAM (1950, 1952, 1959) re- 


ported that the tropics extended somewhat northward of 
49°N latitude along the Pacific coast of North America 
during most of the Eocene. 

Abbreviations used for catalog and/or locality numbers 
are: ANSP, Academy of Natural Sciences of Philadelphia; 
CAS, California Academy of Sciences, San Francisco; 
LACMIP, Natural History Museum of Los Angeles 
County, Invertebrate Paleontology Section; UCMP, Uni- 
versity of California Museum of Paleontology (Berkeley); 
UCR, University of California, Riverside; UWBM, Uni- 
versity of Washington (Seattle), Thomas Burke Memorial 
Washington State Museum (= UW in older literature). 


NEW STRATIGRAPHIC DISTRIBUTION 


The new stratigraphic report in Washington is from the 
Tukwila Formation just south of Seattle (Figure 1). In- 
tensive collecting during a seven-year period (1981-1988) 
by personnel of UWBM yielded 11 specimens of Sulco- 
cypraea mathewsonu (Gabb, 1869). Ten of these specimens 


Page 82 


are from UWBM loc. A7561, informally known as the 
Poverty Hill site. They supplement a single specimen col- 
lected by C. E. Weaver from UWBM loc. 11, essentially 
equivalent to UWBM loc. A7561. Weaver’s specimen is 
deposited also at UWBM. A twelfth specimen is from 
UWBM loc. 229 in the immediate vicinity of UWBM loc. 
A7561. The specimens are internal molds for the most 
part, but eight of them do retain some remnants of shell 
material. 

Sedimentary rocks in the Poverty Hill area south of 
Seattle have been mapped as the Tukwilla [szc] Formation 
by McWILLIAMS (1971). Fossils in this area are found in 
current-concentrated shell beds that are interstratified with 
poorly sorted, barren basaltic sandstone layers. Mc- 
Williams listed 39 species of shallow-water subtropical 
mollusks from these shell beds, but he did not include 
Sulcocypraea mathewsonu. ARMENTROUT et? al. (1983) cor- 
related the Tukwila Formation to the middle and upper 
Eocene and assigned most of the formation to the Bartonian 
Stage (upper middle Eocene), approximately coeval with 
the Cowlitz Formation in southwestern Washington. 

The 12 specimens from the Tukwila Formation near 
Seattle extend the geographic range of this species north- 
ward about 1100 km. Previously, this species was known 
only as far north as near Martinez, Suisun Bay, Contra 
Costa County, north-central California. 

Specimens only tentatively identified as Sulcocypraea ma- 
thewsonu are recognizable in collections from both north- 
western and southwestern Oregon. A single specimen from 
the Hamlet formation (informal name of NIEM & NIEM, 
1985) near Portland in northwestern Oregon (Figure 1) 
is poorly preserved and only identified as S. cf. S$. mathew- 
sonu. The internal mold was collected by Gregory J. Re- 
tallack in an area known as the Rocky Point quarry locality 
(LACMIP loc. 15649). The fossils are in bouldery rubble 
derived from basaltic headlands and deposited in pocket 
beaches along a storm-dominated rocky coastline 
(MUMFORD & NIEM, 1992). Previous workers (WARREN 
& NORBISRATH, 1946; STEERE, 1957; NIEM & VAN ATTA, 
1973:90) listed as many as 18 species of marine inverte- 
brates from the vicinity of this locality, but no mention 
was made of S$. mathewsonu. The strata at this locality 
were formerly regarded by these previous workers as part 
of the Cowlitz or Goble formations, but MUMFORD & 
NiEM (1992) correlated the fossiliferous basaltic conglom- 
erate to the basal Roy Creek member of the Hamlet for- 
mation. They reported abundant calcareous nannofossils 
indicative of the CP14a and CP14b Zones from the upper 
part of the Hamlet formation. AUBREY et al. (1988) as- 
signed these zones to the late middle Eocene. The age of 
the Sulcocypraea specimen, which is from beds lower in 
the Hamlet formation, is herein regarded as approximately 
late middle Eocene in age. 

Another single, poorly preserved specimen tentatively 
identified as Sulcocypraea cf. S. mathewsonu is from the 
Tyee Formation in southwestern Oregon (Figure 1). This 
locality, informally known as the Comstock overpass lo- 


The Veliger, Vol. 36, No. 1 


Seattle 
4 Tukwila Fm. 


Hamlet fm. 


Portland 
OREGON 


A Tyee Fm. 


CALIFORNIA 


Muir 
O Sandstone 


San Francisco 


oO 
Q 
ay 
Zz 


tc Tejon Fm. 
A Juncal Fm. 


Los Angeles 
A NEW LOCALITIES 


O PREVIOUS LOCALITIES 
0 200 km 


Figure 1 


Index map of new and previous localities of Sulcocypraea ma- 
thewsoni (Gabb, 1869). 


cality (UCMP loc. A-1134), was first mentioned by DIL- 
LER (1896:460). TURNER (1938:19) recorded an inverte- 
brate fauna of more than 20 species from this locality and 
identified one of the species as Cypraea sp. B. It is based 
on a single specimen of Sulcocypraea cf. S. mathewsoni that 
consists of an internal mold with only a small remnant of 


R. L. Squires & L. T. Groves, 1993 


Explanation of Figures 2 to 4 


Figures 2-4. Sulcocypraea mathewsonu (Gabb, 1869), hypotype 
UWBM 22052 from UWBM loc. A7561, internal mold, x 3.3. 
Figure 2: apertural view. Figure 3: abapertural view. Figure 4: 
right lateral view. 


shell in the posterior outer lip area. HOOVER (1963), who 
did detailed geologic mapping in the area, gave an updated 
version of Turner’s check list from UCMP loc. A-1134 
and mentioned Cypraea sp. B of Turner. The locality was 
shown by HOOVER (1963) to be in the Tyee Formation. 
He also listed a microfossil assemblage from this locality 
and mentioned that the microfauna is similar to that of 
the Elkton siltstone member of the Tyee Formation in the 
lower Umpqua River area, Oregon. Recent workers (HEL- 
LER & DICKINSON, 1985; MOLENAAR, 1985) interpreted 
the depositional setting of the stratigraphically complex 
Tyee Formation to be a delta-fed submarine fan and as- 
signed the formation to the middle Eocene. 

A new record of Sulcocypraea mathewsonu in southern 
California was detected in the UCR invertebrate pale- 
ontology collection. It is a single specimen from UCR loc. 
4750 in the upper half of the Juncal Formation in the 
Pine Mountain area, Ventura County, southern Califor- 
nia. The specimen was collected from a lens of conglom- 
eratic sandstone by GIVENS (1974) but not mentioned by 
him in his study of the fauna. The locality, situated at the 
boundary between sandstone (inner sublittoral) and silt- 
stone (inner sublittoral to deltaic complex), was assigned 
by GIVENs (1974:table 1) to the Turritella uvasana applinae 
faunal zone, or approximately the middle Eocene (“Do- 
mengine Stage’). 


Page 83 


SYSTEMATIC PALEONTOLOGY 
Family OVULIDAE Fleming, 1828 
Subfamily EOCYPRAEINAE Schilder, 1924 
Genus Sulcocypraea Conrad, 1865 


Type species: Cypraea lintea Conrad, 1847 [1848], by 
monotypy, lower Oligocene (Rupelian Stage), Byram For- 
mation, Vicksburg Group, Mississippi. 


Remarks: Because SCHILDER (1924, 1927) and SCHILDER 
& SCHILDER (1971) assigned Sulcocypraea to the subfamily 
Eocypraeinae, family Amphiperatidae (= Ovulidae) we 
have provisionally followed their classifications. However, 
the morphology of most fossil genera of Eocypraeinae sug- 
gest that they belong within the family Cypraeidae, a 
concept that is beyond the scope of this paper. 


Sulcocypraea mathewsonu (Gabb, 1869) 
(Figures 2-4) 


Cypraea (Epona) mathewsoni GABB, 1869:164, 225, pl. 27, 
figs. 44a, b; ARNOLD, 1906:15; KEEN & BENTSON, 1944: 
152. 

Cypraea mathewsonn Gabb, 1869: WHITEAVES, 1895:128; 
DICKERSON, 1916:421, 438, 448; ANDERSON & HANNA, 
1925:43, 107; NELSON, 1925:425; STEWART, 1926 [1927]: 
371, pl. 28, fig. 5; INGRAM, 1942:105, pl. 2, figs. 10- 
11; INGRAM, 1947a:61; INGRAM, 1947b:147; WEAVER, 
1953:43; RICHARDS, 1968:156. [Non DicKERSON, 1915: 
43, 60, pl. 6, fig. 5a.] 

Cypraea kerniana ANDERSON & HANNA, 1925:43, 104-105, 
107, pl. 13, figs. 9-11; CLARK, 1926:115; HANNA, 1927: 
314, pl. 52, figs. 7, 9; STEWART, 1926 [1927]:371; KEEN 
& BENTSON, 1944:152. 

Sulcocypraea mathewsonu (Gabb, 1869): SCHILDER, 1927:81; 
SCHILDER, 1941:104. 

Sulcocypraea mathewsoni mathewsonu (Gabb, 1869): SCHIL- 
DER, 1932:222; SCHILDER & SCHILDER, 1971:68, 131. 

Sulcocypraea kerniana (Anderson & Hanna, 1925): SCHIL- 
DER, 1932:222; SCHILDER, 1941:104; SCHILDER & 
SCHILDER, 1971:68, 125; DOLIN & DOLIN, 1983:44. 

Cypraea sp. B: TURNER, 1938:19, 35; HOOVER, 1963:27. 

Luponovula mathewsonu (Gabb, 1869): DOLIN & Do Lin, 1983: 
42-45, figs. 28, 29a-c. 


Type material and type locality: Of Cypraea mathew- 
soni, holotype, ANSP 4217; Eocene “Tejon Group” near 
Martinez, Contra Costa County, California (GABB, 1869). 
Of C. kerniana, holotype, CAS 245.02 (ex CAS 816) and 
paratypes, CAS 245.03 and 245.04 (ex CAS 817, 818); 
Grapevine Creek, Kern County, California (CAS loc. 245), 
Eocene “Type” Tejon Formation (ANDERSON & HANNA, 
1925). 


Geographic distribution: Seattle, King County, Wash- 
ington to San Diego, San Diego County, southern Cali- 
fornia. 


Stratigraphic distribution: California “Domengine Stage” 


Page 84 


(middle Eocene part) to “Tejon Stage,” equivalent to mid- 
dle to upper middle Eocene (Lutetian to Bartonian Stages) 
(see SQUIRES, 1988). ‘““DOMENGINE STAGE”: Tentatively 
the Tyee Formation, southwestern Oregon (TURNER, 1938; 
Hoover, 1963); Muir Sandstone, near Martinez, Contra 
Costa County, north-central California (WEAVER, 1953); 
upper Juncal Formation, Pine Mountain area, southern 
California (herein); Rose Canyon Shale Member, La Jolla 
Formation [= Ardath Shale] (DICKERSON, 1916; CLARK, 
1926; HANNA, 1927). ““TEJON STAGE”: Tukwila Forma- 
tion, Seattle, Washington (herein); tentatively the Hamlet 
formation (informal), northwestern Oregon (herein). 
‘““‘DOMENGINE STAGE’’/‘“‘TEJON STAGE” UNDIFFER- 
ENTIATED: “Tejon Group,” Eocene, near Martinez, Con- 
tra Costa County, north-central California (GABB, 1869; 
ARNOLD, 1906; STEWART, 1926 [1927]; SCHILDER, 1932; 
INGRAM, 1942; RICHARDS, 1968); “Type” Tejon Forma- 
tion, Grapevine Canyon area, south-central California 
(GABB, 1869; DICKERSON, 1915; DICKERSON, 1916; 
ANDERSON & HANNA, 1925; CLARK, 1926). 


Remarks: Because of morphologic similarities, Sulcocy- 
praea kerniana was judged by SCHILDER & SCHILDER (1971) 
to be a primary junior synonym of S. mathewsonu. 

The only other species of Sulcocypraea known from the 
Pacific coast of North America is Cypraea oakvillensis Van 
Winkle, 1918, based on a single specimen from UWBM 
loc. 169 in the Eocene-Oligocene Lincoln Creek Forma- 
tion, near Oakville, Grays Harbor County, western Wash- 
ington, approximately 105 km southwest of Seattle. VAN 
WINKLE (1918) assigned C. oakvillensis to the Barbatia 
merriami zone, which ARMENTROUT (1975: fig. 2) corre- 
lated with the uppermost Eocene Echinophoria dalli zone 
of the Pacific Northwest Galvinian Stage. Sulcocypraea 
oakvillensis was treated as a subspecies of S. mathewsonn 
by SCHILDER & SCHILDER (1971), but the holotype (CAS 
61715.01 [ex UWBM 140)}) of S. oakvillensis was too poorly 
preserved to justify this assignment. The holotype of S. 
oakvillensis is now missing, and the available illustrations 
(VAN WINKLE, 1918:pl. 7, fig. 19; INGRAM, 1942:pl. 2, 
figs. 14-15; 1947a:pl. 2, figs. 15-16; WEAVER, 1942 [1943]: 
pl. 76, figs. 29-30) are unsatisfactory because of the poor 
preservation. Until additional topotypes of S$. oakvillensis 
are found, which seems unlikely due to poor exposures in 
the area (W. C. Wehr, personal communication), the name 
should be treated as a nomen dubium. 

Five species of Sulcocypraea are known from the Gulf 
coast of North America. Sulcocypraea perinflata (Schilder, 
1927), from Alabama, is the earliest species of the genus. 
HarRIs (1896) reported this species from “upper Lignitic”’ 
strata at Woods Bluff on the Tombigbee River, Clarke 
County, Alabama, but he mistakenly referred to the species 
as Cypraea smithu Aldrich, 1886. TOULMIN (1977) placed 
the Woods Bluff locality in the lower Eocene Bashi Mar] 
Member of the Hatchebigee Formation, and DOCKERY 
(1986) assigned the Bashi Marl Member to the lowermost 


The Veliger, Vol. 36, No. 1 


Eocene. Other described species are Sulcocypraea kennedyi 
(Harris, 1895) from the middle Eocene of Mississippi, 
Texas, and South Carolina; S. vaughani (Johnson, 1899) 
from the upper Eocene of Mississippi, Louisiana, and 
South Carolina (PALMER & BRANN, 1966; DOCKERY, 1980); 
and S. lintea (Conrad, 1847 [1848]) and S. healey: (Aldrich, 
1923) [= S. dalli (Aldrich, 1894), preoccupied] from the 
lower Oligocene of Mississippi and Mississippi and Lou- 
isiana, respectively (MACNEIL & DOCKERY, 1984). 

The only South American species of Sulcocypraea is 
Amphiperas bullennewtoni Olsson, 1930, from the middle 
Eocene Talara Formation, at Yasila, Piura Dept., Peru 
(BRANN & KENT, 1960). The only species of Sulcocypraea 
known from anywhere else in the world is one morpho- 
logically close to S. mathewsonu from Eocene rocks near 
Pau, Pyrenees-Atlantiques, in the Bearn Basin of south- 
western France (DOLIN & DOLIN, 1983). 

A review by Groves (in preparation) of Sulcocypraea 
suggests that all of the northeastern Pacific species of this 
genus and the southwestern France species may belong to 
a new subgenus of Sulcocypraea. Species from the Gulf 
coast and Peru appear to belong to Sulcocypraea, sensu 
stricto. 

The geologic range of Sulcocypraea was previously re- 
ported to be middle Paleocene to late Oligocene (WENZ, 
1941; SCHILDER & SCHILDER, 1971) but is refined herein 
to range from the earliest Eocene to early Oligocene. 


ACKNOWLEDGMENTS 


We thank James L. Goedert (Gig Harbor, Washington) 
for informing us about the Tukwila Formation ovulid 
specimens and for information about the Rocky Point lo- 
cality. Wesley C. Wehr (UWBM) kindly located all the 
Poverty Hill specimens and enthusiastically supplied much 
information about the associated molluscan fauna. He and 
V.S. Mallory (UWBM) provided casts of the holotype of 
Sulcocypraea oakvillensis. Ronald C. Eng (UWBM) efh- 
ciently provided for the loan of the specimens. 

Elana Benamy (Academy of Natural Sciences of Phil- 
adelphia), Michael G. Kellogg (CAS), Marilyn A. Kooser 
(UCR), Peter Hoover (Paleontological Research Institu- 
tion, Ithaca, New York), and David R. Lindberg and Rex 
A. Hanger (UCMP) loaned specimens under their care. 

Gregory J. Retallack (Department of Geological Sci- 
ences, University of Oregon) donated the specimen from 
Rocky Point quarry to LACMIP and shared his know]l- 
edge of the geology of the locality. Wendy A. Niem (De- 
partment of Geosciences, Oregon State University) shared 
her knowledge of the outcrop distribution of the Hamlet 
formation. 

George L. Kennedy (LACMIP), James H. McLean 
(Natural History Museum of Los Angeles County, Mal- 
acology Section), and two anonymous reviewers critically 
read the manuscript. 


R. L. Squires & L. T. Groves, 1993 


LOCALITIES CITED 


CAS loc. 245. Along the east bank of a small gulch about 
0.4 km E of the pumping plant located near the mouth 
of Grapevine Creek, Kern County, California 
(ANDERSON & HANNA, 1925:39). “Type” Tejon For- 
mation (in the broad sense). Age: Middle to possibly 
late middle Eocene. Collector: B. G. Martin. 

LACMIP loc. 15649. Rocky Point quarry, also known as 
the Columbia County quarry, (= Stop 5 of STEERE, 
1957:40, and Stop 1-3 of NIEM et al., 1973:99-100, 
fig. 3), at end of access road 0.2 km W of Timber- 
Vernonia road 10.5 km SW of Vernonia or 9.4 km 
N of junction on State Highway 26 and Timber- 
Vernonia road, in E central part of section 22, T4N, 
R5W, U.S. Geological Survey, 7.5-minute, Clear 
Creek, Oregon, quadrangle, 1979, Columbia County, 
northwestern Oregon. Basalt is exposed at base of 
abandoned quarry, but overlying the basalt is about 
5 m of basal conglomerate containing many marine 
fossils. Locality approximately same as LACMIP loc. 
5887. Basal Roy Creek member of the Hamlet for- 
mation (informal names). Age: Late middle Eocene. 
Collector: G. J. Retallack. 

UCMP loc. A-1134. Comstock overpass locality (= locality 
M-12 of Hoover, 1963:26, pl. 1), in road-cut at E 
end of old Pacific Highway overpass at old railroad 
siding 0.8 km S of Comstock (TURNER:1938, fig. 5), 
NE" section 20, T21S, R4W, U.S. Geological Sur- 
vey, 7.5-minute, Curtin, Oregon, quadrangle, provi- 
sional edition 1987, Douglas County, southwestern 
Oregon. Tyee Formation. Age: Middle Eocene. Col- 
lector: F. E. Turner, 1938. 

UCR loc. 4750. On crest of ridge 823 m (2700 ft) W of 
elevation 6200 on San Guillermo Mountain (see GI- 
VENS, 1974:100 and geologic map), 152 m (500 ft) N, 
213 m (700 ft) W of SE corner of section 13, T7N, 
R22W, U.S. Geological Survey, 7.5-minute, San 
Guillermo, California, quadrangle, 1943, Ventura 
County, southern California. Age: Middle Eocene. 
Collector: C. R. Givens, 1974. 

UWBM loc. 11. In sandstone at NE corner of rock outlier 
at Duwamish station, section 10, T24N, R4E, U.S. 
Geological Survey, 7.5-minute, Seattle South, Wash- 
ington, quadrangle, 1949 (photorevised 1968 and 
1973), King County, western Washington. Same as 
UWBM loc. A7561. Tukwila Formation. Age: Late 
middle Eocene. Collector: C. E. Weaver, 1909. 

UWBM loc. 169. Oakville quarry, in sandstone overlying 
basalt, 1.6 km W of Oakville, on Burlington Northern 
railroad track, section 19, T16N, R4W, U.S. Geo- 
logical Survey, 15-minute, Rochester, Washington, 
quadrangle, 1953, Grays Harbor County, western 
Washington. Lincoln Creek Formation. Age: Latest 
Eocene. Collector: K. E. H. Van Winkle, 1918. 

UWBM loc. 229. Approximately 600 m N22°E from UW 
loc. A7561 (see below) in section 3, T23N, R4E, (see 


Page 85 


McWILLIAMS, 1971:fig. 1), N side of Duwamish Riv- 
er area, S of Seattle, King County, Washington, U.S. 
Geological Survey, 7.5-minute, Seattle South, Wash- 
ington, quadrangle, 1949 (photorevised 1968 and 
1973), King County, western Washington. Tukwila 
Formation. Age: Late middle Eocene. Collector: V. S. 
Mallory. 

UWBM loc. A7561. Poverty Hill, S of Boeing Field, where 
NE corner of the hill in section 10 intersects the section 
boundary between sections 3 and 10 in T23N, R4E, 
N side of Duwamish River area, approximately 0.4 
km W of intersection of Interstate Highway 5 and 
Martin Luther King Way (formerly Empire Way), 
U.S. Geological Survey, 7.5-minute, Seattle South, 
Washington, quadrangle, 1949 (photorevised 1968 and 
1973), King County, western Washington. Same as 
UWBM loc. 11. Tukwila Formation. Age: Late mid- 
dle Eocene. Collectors: C. E. Weaver, 1909; Eric 
Brown, Terrence Frest, Edward Johannes, V.S. Mal- 
lory, Mark Reeves, N. Smith, Ted Weasma, and W. 
C. Wehr, 1981-1988. 


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THE VELIGER 
© CMS, Inc., 1993 


The Veliger 36(1):88-91 (January 4, 1993) 


New Records for Ranellid Gastropods in the 
Western Atlantic (Ranellidae: Cymatiinae) 
by 


BETTY JEAN PIECH 


Associate in Malacology, Delaware Museum of Natural History, 
Wilmington, Delaware 19807, USA 


Abstract. Additional confirmation is given for the presence of Cymatium (Monoplex) mundum (Gould, 
1849) in the western Atlantic. Cymatium (Turritriton) vespaceum (Lamarck, 1822) is authenticated from 
Florida and Honduras; Cymatium (Reticutriton) pfeifferianum (Reeve, 1844) is reported for the first 
time from Florida and Brazil; and Cymatium (Ranularia) gallinago (Reeve, 1844) is reported from Brazil. 


INTRODUCTION 


Although several prosobranch gastropod families have spe- 
cies with teleplanic larvae, such species are especially com- 
mon in Ranellidae. Some of these larvae are very long- 
lived and this enables them to disperse over a large area. 
During recent examinations of private and museum col- 
lections and a collecting trip to Brazil, I found specimens 
that confirmed and extended the ranges of the species cited 
herein. 

Collections studied are as follows: AMNH—American 
Museum of Natural History, New York, New York; 
DMNH—Delaware Museum of Natural History, Wil- 
mington, Delaware; Garcia Coll.—Dr. E. F. Garcia, La- 
fayette, Louisiana; NHM(L)—The Natural History Mu- 


seum, London (formerly the British Museum [Natural 
History]); Piech Coll.—B. J. Piech, Wilmington, Dela- 
ware; Sunderland Coll.—Kevan and Linda Sunderland, 
Sunrise, Florida; Trinchao Coll.—Luiz Trinchao, Sal- 
vador, Bahia, Brazil; Voss Coll.—Carolyn Voss, Ham- 
mond, Louisiana. 


WESTERN ATLANTIC RECORDS oF 
FOUR SPECIES or RANELLIDAE 
Cymatium (Monoplex) mundum (Gould, 1849) 
(Figures 1, 2) 


In the past, Cymatium mundum was usually placed in 
synonymy with Cymatium (Monoplex) gemmatum (Reeve, 


Explanation of Figures 1 to 16 


Figures 1-16. Cymatium. Photography by the author. 


Figure 1. Cymatium mundum; Sunderland Coll.; Key West, Florida; 38 mm. 


Figure 2. C. mundum; Sunderland Coll.; Key West, Florida; 29 mm. 


Figure 3. C. vespaceum; Piech Coll.; Roatan, Honduras; 41 mm. 


Figure 4. Dorsal view of Figure 3. 


Figure 5. C. vespaceum; Sunderland Coll.; Key Largo, Florida; 22 mm. 


Figure 6. Dorsal view of Figure 5. 


Figure 7. C. pfeifferianum; Voss Coll.; Todos Santos Bay, Bahia, Brazil; 46 mm. 


Figure 8. Dorsal view of Figure 7. 


Figure 9. C. pfeifferianum; Piech Coll.; Australia; 60 mm. 


Figure 10. Dorsal view of Figure 9. 


Figure 11. C. gallinago; figured syntype, NHM(L), No. 1967593; 61 mm. 


Figure 12. Dorsal view of Figure 11. 


Be peeiech 1993 Page 89 


Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 


Figure 7 Figure 8 Figure 9 Figure 10 


Figure 15 Figure 16 


Figure 11 Figure 12 Figure 13 Figure 14 


Figure 13. C. gallinago; Piech Coll.; Todos Santos Bay, Bahia, Brazil; 61 mm. 
Figure 14. Dorsal view of Figure 13. 

Figure 15. C. gallinago, Piech Coll.; Madagascar; 49 mm. 

Figure 16. Dorsal view of Figure 15. 


Page 90 


1844). Then Beu (1985:58) listed both species as valid 
and this was later confirmed by EMERSON (1991:63). Cy- 
matium mundum is very common in the Indo-Pacific but 
only two specimens have been previously recorded from 
the western Atlantic (EMERSON, 1991:65). Here two ad- 
ditional records (3 specimens) from that area are reported. 


(1) AMNH: No. 181298, 1 specimen; Frank Lyman 
Family, 1940 (as “Cymatium vespaceum,” originally 
labeled as “Cymatium gracilis, extremely rare,” dredged 
149 m, off Palm Beach County, Florida; 25 mm. 

(2) Sunderland Coll.: 2 specimens; from shrimp boats, 
1978; 185 m, off Key West, south of the Dry Tortugas, 
Florida; 29 mm (with operculum) and 38 mm. 


It has been suggested that C. mundum might be only a 
shallow-water form of a deep-water C. gemmatum. These 
deep-water specimens of C. mundum, taken in 149 m and 
185 m, refute that idea. 


Cymatium (Turritriton) vespaceum 


(Lamarck, 1822) 
(Figures 3-6) 


Until recently, Cymatium vespaceum was considered a valid 
species in most of the tropical areas of the world including 
the western Atlantic. ABBOTT (1974:163, fig. 1754 [sic; = 
1755]) showed a specimen from that area (Matanzas, 
Cuba), copying the figure cited by CLENCH & ‘TURNER 
(1957:223, pl. 125, fig. 1) as C. gemmatum. Actually those 
figures appear to show what is now called Cymatium (Tur- 
ritriton) comptum (A. Adams, 1854) since BEU (1985:60) 
has separated C. comptum from C. vespaceum, placing the 
former in the Indo-Pacific and eastern and western At- 
lantic, and restricting C. vespaceum to the Indo-Pacific. 

My subsequent examination of numerous specimens la- 
beled as Cymatium vespaceum from the western Atlantic 
confirmed that most of them should be referred to C. comp- 
tum. However, two specimens of C. vespaceum from that 
area have been verified, so the western Atlantic must be 
included in its range. 


(1) Piech Coll.: 1 specimen; self-collected, crabbed, May 
1980; Roatan Island, Honduras; 41 mm. 

(2) Sunderland Coll.: 1 specimen (juvenile); self-collected, 
dead, 1978; 4.5 m, Pickle’s Reef off Key Largo, Flor- 
ida; 22 mm. 


Cymatium (Reticutriton) pfeifferanum (Reeve, 1844) 
(Figures 7—10) 


This Cymatium species previously had been reported only 
from the Indo-West Pacific (BEU, 1985:59). As a result of 
my recent examination of the five western Atlantic spec- 
imens listed below, the range of C. pfezfferianum should 
now include that area. 


(1) DMNH: No. 74116, 2 very juvenile but identifiable 


specimens; ex J. W. Poling, 16 February 1971; 46 m, 
W of Egmont Key, Florida; 10 mm and 28 mm. 


The Veliger, Vol. 36, No. 1 


(2) Trinchao Coll.: 2 specimens, not measured; self-col- 
lected, dead, no date; Todos Santos Bay, Bahia, Brazil. 
(3) Voss Coll.: 1 specimen; self-collected, dead, 1979-1980; 
beachwash, Todos Santos Bay, Bahia, Brazil; 46 mm. 


As additional confirmation, I recently had the oppor- 
tunity to talk with Professor Eliézer de C. Rios (1992) 
and see the manuscript of his up-coming book Seashells of 
Brasil, 2nd ed. The following is an excerpt from page 121: 
“Cymatium pfeifferianum (Reeve, 1844) Australia to Ja- 
pan, Philippines Is.—Northeast Brasil. . . . Only Brasilian 
record: Itaparica Is., Bahia, from hermit-crabs (B. Lin- 
hares).” 


Cymatium (Ranularia) gallinago (Reeve, 1844) 
(Figures 11-16) 


REEVE (1844:pl. II, sp. 5) and BEu (1985:59) list Cyma- 
tum gallinago as a western Pacific species, although all 
the specimens that I have examined previously have been 
from the Indian Ocean. Seven specimens from Brazil are 
reported here and that country must now be included in 
its range. 

These seven specimens, listed below, were misidentified 
as Cymatium (Ranularia) trilineatum (Reeve, 1844). After 
comparison with Reeve’s syntypes of these two species that 
were borrowed from NHM(L) (C. trilineatum No. 1967627 
and C. gallinago No. 1967593), all seven specimens are 
definitely referable to C. gallinago. 


(1) Garcia Coll.: 1 specimen; self-collected, dead, August 
1991; beachwash, Itaparica Island, Todos Santos Bay, 
Bahia, Brazil; 62 mm, siphonal canal broken. 

(2) Piech Coll.: 1 specimen; collected by Luiz Trinchao, 
dead, no date; Todos Santos Bay, Bahia, Brazil; 61 
mm. 

(3) Piech Coll.: 1 specimen; self-collected, dead, August 
1991; beachwash, Itaparica Island, Todos Santos Bay, 
Bahia, Brazil; 34 mm, siphonal canal broken. 

(4) Trinchao Coll.: 2 specimens; self-collected, dead, no 
date; Todos Santos Bay, Bahia, Brazil; not measured. 

(5) Voss Coll.: 2 specimens; self-collected, dead, 1979- 
1980; beachwash, Todos Santos Bay, Bahia, Brazil; 
53 mm and 54 mm, larger one with broken siphonal 
canal. 


ACKNOWLEDGMENTS 


I would like to express my appreciation to Dr. E. F. Garcia, 
Kevan and Linda Sunderland, and Carolyn Voss for fur- 
nishing specimens for study; to Kathie Way, NHM(L), 
for loaning syntypes; and to Mary Jane Arden, DMNH, 
for her assistance with graphics. Dr. A. G. Beu, DSIR 
Geology and Geophysics, Lower Hutt, New Zealand, and 
Dr. William Emerson and Walter Sage III, AMNH, re- 
viewed my manuscript and offered many helpful sugges- 
tions. I thank them and the other reviewers for their con- 
structive comments. A special note of credit and appreciation 


Ben ebiech 993 


Page 91 


must go to Luiz Trinchao of Salvador, Bahia, Brazil, for 
calling to my attention the occurrence of Cymatium pfezf- 
ferianum and C. gallinago in his country. 


LITERATURE CITED 


ABBOTT, R. T. 1974. American Seashells. 2nd ed. Van Nos- 
trand Reinhold Co.: New York. p. 163-164. 

BEu, A. G. 1985. A classification and catalogue of living world 
Ranellidae (=Cymatiidae) and Bursidae. Conchologists of 
America Bulletin 13(4):55-66. 

CLENCH, W. J. & R. D. TURNER. 1957. The family Cymatiidae 
in the western Atlantic. Johnsonia 3(36):189-244. 


EMERSON, W. K. 1991. First records for Cymatiwm mundum 
(Gould) in the eastern Pacific Ocean, with comments on the 
zoogeography of the tropical trans-Pacific tonnacean and 
non-tonnacean prosobranch gastropods with Indo-Pacific 
faunal affinities in West American waters. Nautilus 105(2): 
62-80. 

REEVE, L. A. 1844. Monograph of the genus 7riton. Con- 
chologia Iconica: Illustrations of molluscan animals. Reeve 
Brothers: London. 2 Triton text and 20 pls. 

Rios, ELIEZER DEC. 1992. Museu Oceanographico, Rio Gran- 
de, RS, Brasil. Manuscript of soon-to-be-published Seashells 
of Brasil. 2nd ed. 


The Veliger 36(1):92-97 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


NOTES, INFORMATION & NEWS 


Predation by Latiaxis oldroydi 
(Gastropoda: Coralliophilidae) on 
Corynactis californica 
(Anthozoa: Corallimorphidae) 
by 
Mary K. Wicksten and Robert T. Wright 
Department of Biology, Texas A&M University, 
College Station, Texas 77843, USA 


The subtidal gastropod Latiaxis oldroydi (I. Oldroyd, 1929) 
ranges from Point Conception, California, to Cedros Is- 
land, Baja California, Mexico (MCLEAN, 1978). 
ROBERTSON (1970) reported that species of the family Cor- 
alliophilidae usually are suctorial predators on stony cor- 
als, although a few species also were reported to feed on 
gorgonians, zoanthids, antipatharians, and alcyonarians. 

On 15 December 1990, one of us (MKW) collected two 
specimens of Latiaxis oldroydi at 10 m on rocks near Indian 
Rock, Santa Catalina Island, California. These mollusks 
were transported to Texas A&M University and kept in 
a refrigerated marine aquarium at 10°C. Inactive and 
heavily encrusted with coralline algae, the two specimens 
mostly went unnoticed. However, in fall 1991, a cluster 
of the “strawberry anemone” Corynactis californica Carl- 
gren, 1936 (actually a member of the order Corallimor- 
pharia) was added to the tank. We noticed that the L. 
oldroydi crawled to the cluster, and that bare patches ap- 
peared among the anemones. 

From 27 January to 6 May 1992 we kept records of 
the movements of the two Latiaxis oldroydi and the numbers 
of Corynactis californica. During that time, the mollusks 
ate 16 anemones, averaging one anemone per mollusk per 
week (range 0-3 anemones per week). During much of 
the time, the mollusks remained almost motionless, but 
one moved 7 cm in a single day. The anemones did not 
present any noticeable escape responses, such as crawling 
on the pedal disk, detaching from the substrate, or at- 
tempting to sting, although one anemone removed itself 
from harm’s way by attaching to the dorsal surface of a 
mollusk’s shell. 

Members of the Coralliophilidae have not been reported 
previously to feed on corallimorpharians. Due to its rel- 
atively strong stinging cells, Corynactis californica appar- 
ently has few predators. The leather starfish Dermasterias 
imbricata (Grube, 1857) will consume strawberry anem- 
ones, although it seems to prefer other species of antho- 
zoans as prey if it has access to them (ANNETT AND PI- 
EROTTI, 1984). 

In nature, it is likely that Latzaxis oldroydi also feeds on 
the ahermatypic coral Astrangia lajollaensis Durham, 1947, 
which is common in the areas it inhabits. It also may feed 
on the corals Paracyathus stearnsi Verrill, 1869, and Coeno- 
cyathus bowersi Vaughan, 1906, which live in subtidal rocky 
areas off southern California. 


Literature Cited 


ANNETT, C. & R. PIEROTTI. 1984. Foraging behavior and prey 
selection of the leather seastar Dermasterias imbricata. Marine 
Ecology Progress Series 14:197-206. 

McLEan, J. H. 1978. Marine shells of southern California. 
Los Angeles County Natural History Museum Science Se- 
ries 24:1-104. 

ROBERTSON, R. 1970. Review of the predators and parasites 
of stony corals, with special references to symbiotic proso- 
branch gastropods. Pacific Science 24:43-54. 


Invasion of the South Texas Coast by the 
Edible Brown Mussel Perna perna 
(Linnaeus, 1758) 
by 
David W. Hicks and John W. Tunnell, Jr. 
Center for Coastal Studies, 

Corpus Christi State University, 

6300 Ocean Drive, 

Corpus Christi, Texas 78412, USA 


Biological invasion as defined by CARLTON (1987) is the 
arrival, establishment, and diffusion of a species. Biological 
invasions in natural marine communities occur through 
two processes, range expansions and introductions 
(CARLTON, 1987). Range expansions consist of dispersal 
by natural mechanisms into a region where the species did 
not formerly exist. Introductions consist of transportation 
by human activity into a region where the species did not 
formerly exist. Introductions of exotic organisms have been 
linked to fouling and boring communities on ships, ballast 
seawater from ships, semi-submersible exploratory drilling 
platforms, and fisheries introductions (CARLTON, 1987). 
Carlton tallied the number of introduced mollusks within 
North America at the National Shellfisheries Association 
meeting in April of 1990 (CHEW, 1990). The Pacific coast 
of North America accommodated nearly 40 non-native 
species, the Atlantic coast 10 or fewer, and the Gulf coast 
five or fewer. 

The introduction of nonindigenous species can have dev- 
astating impacts on native ecosystems. The Asiatic clam 
(Corbicula fluminea Miller, 1774), inadvertently intro- 
duced into the United States in the 1930s, has spread to 
35 states, colonizing all of the major Pacific and Atlantic 
river drainages (BRITTON & MorTon, 1979; Isom, 1986). 
Corbicula fluminea has since become a pest organism be- 
cause of biofouling in water treatment facilities, irrigation 
systems, and power generating stations (KING et al., 1986). 
Another recent account of a biological invader arriving in 
the United States is the zebra mussel (Dreissena polymorpha 
Pallas, 1754). This small, freshwater mollusk has the po- 
tential to spread throughout much of North America and 
create serious problems for various aquatic organisms, par- 


Notes, Information & News 


ticularly native endangered mussels (FRENCH, 1990) while 
also biofouling various water usage facilities. The zebra 
mussel apparently was introduced from Europe acciden- 
tally via the release of ballast water from international 
vessels (FRENCH, 1990). 

Small specimens (2 cm in length) of what was later 
determined to be Perna perna (Linnaeus, 1758) were first 
collected from the Port Aransas Jetty in February 1990, 
following one of the area’s most severe freezes in December 
1989. By December 1991 mussels had successfully colo- 
nized the intertidal zone of the jetty rocks at Port Aransas, 
Fish Pass (Corpus Christi Water Exchange Pass), and 
Port Mansfield Pass. The Port Aransas and Port Mans- 
field jetties are 230 km apart. In areas of noted coloni- 
zation, mussel densities are as high as 50 individuals per 
quarter meter square. Due to mussel colony locations on 
jetty rocks that protect the entrances of bays, they are in 
good proximity to propagate themselves further into their 
respective bays wherever hard substrates are available. 

Perna perna is common to the Atlantic coast of South 
America from Venezuela to Uruguay (Rios, 1975, 1985; 
BAYNE, 1976), the southern coasts of Africa from Walvis 
Bay to Mozambique (KENNELLY, 1969), India, and Sri 
Lanka (VAKILY, 1989). Eleven synonyms for P. perna were 
cited by SIDDALL (1980). The genus Perna is characterized 
by the anterior position of the pedal retractor muscle, wide- 
ly separated posterior retractor muscles, the absence of any 
anterior adductor muscle, and the often green color of the 
shell (Rios, 1975; BAYNE, 1976). Because of the degree of 
variation in characters of taxonomic importance within the 
genus Perna, it is difficult to distinguish reliably among 
species without knowing from what locality they were 
collected (SIDDALL, 1980). Perna perna is described as up 
to 170 mm long (90 mm average) and smooth with con- 
centric growth lines; it has a purple nacreous interior, and 
the ventral margin is straight with one or two teeth. The 
periostracum is dark brown with yellow-greenish bands 
near the ventral margin (Rios, 1975, 1985). The most 
reliable anatomical character used to distinguish P. perna 
from other members of the genus is the presence of enlarged 
sensory papillae along the mantle margins (SIDDALL, 1980). 
Larval surveys in Venezuela indicate as many as three 
prominent spawning peaks for P. perna (VAKILY, 1989). 
Description of the larvae and dissoconch are given by MAR- 
TINEZ (1967). 

Perna perna isa ciliary-mucoid filter feeder that occupies 
the littoral and sublittoral zones, where it, like the zebra 
mussel, attaches by means of byssal threads to a large 
variety of substrates (VAKILY, 1989). Perna perna tolerates 
fairly large fluctuations in salinity, adapting well in ranges 
of 19-44 ppt. Members of the genus Perna exhibit some 
sexual dimorphism. The sexes of truly mature animals can 
often be determined by the color of the gonads, milky to 
creamy white indicating a male and orange to red-orange 
indicating a female. 

Cultivation of Perna perna has been attempted with 
limited success in Venezuela (BAYNE, 1976), where it is 
given the common name “Mexilhao.” Sporadic outbreaks 


Page 93 


of paralytic shellfish poisoning in the 1970s, resulting in 
human deaths, may have contributed to the decline of the 
fishery there (H. H. Hildebrand, personal communica- 
tion). 

The possible sources that could have resulted in the 
introduction of Perna perna, in addition to those previously 
mentioned, include the importing of live shellfish sold in 
local seafood markets. Perna perna was observed live in 
seafood markets in California (J. C. Britton, personal com- 
munication). Local seafood markets also import live mus- 
sels; however, only Mytilus spp. have been encountered. It 
is also noteworthy that the ships of a resident Venezuelan 
oil refining company, Champlin, frequent the Corpus 
Christi Bay area. Perna spp. have been previously docu- 
mented as fouling organisms on the hulls of ships (CARLTON, 
1987). The planktotrophic larvae of this mussel remains 
free-swimming for 15 to 20 days (VAKILY, 1989); thus 
transportation of the organism in ballast water is clearly 
a possibility. It is common practice for international vessels, 
including those from South America, to release ballast 
seawater in nearshore and inshore waters (Harbormaster’s 
Office, Port of Corpus Christi Authority). 

Shellfish introductions may also result in the inadvertent 
introduction of pathogens, algal cysts, and disease organ- 
isms of commercial mollusks (CARLTON, 1989; SHUMWAY, 
1989). Toxic algal blooms occur all over the world and it 
appears the incidence and diversity of blooms has been 
increasing in recent years (SHUMWAY, 1989). There is 
increasing evidence that toxic species are being transported 
to new areas via the translocation of infected shellfish, 
which may result in the release of cysts or motile cells that 
may seed a future bloom in the area of translocation 
(SHUMWAY, 1989). The rate at which shellfish accumulate 
and release toxins is species specific and varies with season 
and the site of toxin storage within the animal (SHUMWAY, 
1989). Besides the potential danger of introducing diseases, 
the remarkable adaptability of Perna to different environ- 
ments could easily lead to undesirable changes in ecological 
equilibria (VAKILY, 1989). 

Voucher specimens of Perna perna, collected from Cor- 
pus Christi, have been deposited at the National Museum 
of Natural History, Smithsonian Institution (USNM No. 
869530) and are also present in the Corpus Christi State 
University Collection. 


Acknowledgments 


We thank T. R. Waller of the Smithsonian Institution for 
confirmation of the species, and H. H. Hildebrand and J. 
C. Britton for providing helpful comments and literature. 


Literature Cited 


Bayn_E, B. L. 1976. Marine Mussels: Their Ecology and Phys- 
iology. Cambridge University Press: Cambridge. 506 pp. 

BRITTON, J.C. & B. MorTON. 1979. Corbicula in North Amer- 
ica: the evidence reviewed and evaluated. Pp. 249-287. In: 
J.C. Britton (ed.), Proceedings, First International Corbicula 
symposium. A Texas Christian University Research Foun- 
dation Publication, Fort Worth, Texas. 


Page 94 


CarLTon, J. T. 1987. Patterns of transoceanic marine biolog- 
ical invasions in the Pacific Ocean. Bulletin of Marine Sci- 
ence 41(2):452-465. 

CARLTON, J. T. 1989. Man’s role in changing the face of the 
ocean: biological invasions and implications for conservation 
of near-shore environments. Conservation Biology 3(3):265- 
PPE 

CHEw, K. K. 1990. Global bivalve shellfish introductions. World 
Aquaculture 21(3):9-22. 

FRENCH, J. R. P., III. 1990. The exotic zebra mussel—a new 
threat to endangered freshwater mussels. Endangered Spe- 
cies Technical Bulletin 15(11):3-4. 

Isom, B. G. 1986. Historical review of Asiatic clam (Corbicula) 
invasion and biofouling of waters and industries in the Amer- 
icas. Proceedings of the Second International Corbicula Sym- 
posium. Special Edition No. 2, American Malacologist Bul- 
letin:1-5. 

KENNELLY, D. H. 1969. Marine Shells of Southern Africa. 
Books of Africa: Cape Town, South Africa. 123 pp. 

Kino, C. A., C. J. LANGDON & C. L. Counts, HI. 1986. 
Spawning and early development of Corbicula fluminea (Bi- 
valvia: Corbiculacea) in laboratory culture. American Mala- 
cologist Bulletin 4(1):81-88. 

MARTINEZ, R. E. 1967. Identification and description of the 
veliconch and dissoconch larvae of the edible mussel, Perna 
perna (L), from eastern Venezuela. Serie Recursos y Ex- 
plotacion Pesqueros 1(3):95-113. 

Rios, E. C. 1975. Brazilian Marine Mollusks Iconography. 
Editora EMMA, Rio Grande-RS, XII, Brazil. 331 pp. 
Rios, E. C. 1985. Coastal Brazilian Seashells. Empresas Ipi- 

ranga, Rio Grande, RS, XI, Brazil. 255 pp. 

SHumMway, S. E. 1989. Toxic algae; a serious threat to shellfish 
aquaculture. World Aquaculture 20(4):65-74. 

SIDDALL, S. E. 1980. A clarification of the genus Perna (My- 
tilidae). Bulletin of Marine Science 30(4):858-870. 

VAKILY, J. M. 1989. The biology and culture of mussels of the 
genus Perna. ICLARM Studies and Reviews 17, Interna- 
tional Center for Living Aquatic Resources Management, 
Manila, Philippines and Deutsche Gesellschaft fur Techni- 
sche Zusammenarbeit (GTZ) GmbH, Eschborn, Federal 
Republic of Germany. 63 pp. 


Brooding of Larvae in Cardita aviculina 
Lamarck, 1819 (Bivalvia: Carditidae) 
by 
Jay A. Schneider 
Department of Geophysical Sciences, 
University of Chicago, 

Chicago, Illinois 60637, USA 


Brooding of larvae in the Carditidae has been known since 
DALL (1903) reported viviparity in Venericardia alaskana 
Dall, 1903 (= Cyclocardia crebicostata (Krause, 1885)) and 
that members of the carditid subfamily Thecaliinae brood 
their young in a marsupium. JONES (1963) described 
brooding in Cyclocardia bailyi (Burch, 1944), C. barbarensis 
(Stearns, 1890), and C. ventricosa (Gould, 1850). YONGE 
(1969) studied brooding in Glans carpenter: (Lamy, 1922) 
and J. A. Allen (personal communication, in YONGE, 1969) 
reported brooding in C. borealis (Conrad, 1831). Brooding 
has been inferred in several species of the extinct genera 
Venericardia (HEASLIP, 1968, 1969) and Vetericardiella 


The Veliger, Vol. 36, No. 1 


(JABLONSKI & LUTZ, 1980, 1983). Here I report the brood- 
ing of larvae in Cardita (Cardita) aviculina Lamarck, 1819. 
Brooded larvae were found in a specimen (Academy of 
Natural Sciences of Philadelphia alcohol collection, 269882) 
from off Poum, southwest New Caledonia. None of the 
other 10 specimens in the lot contained larvae. This is the 
first report of brooded larvae in Cardita, sensu stricto, since 
all other species of Cardita in which brooding has been 
reported have been reassigned to either Cyclocardia or Glans. 

The larvae are identical to what both JONEs (1963) and 
YONGE (1969) considered the 1a stage of larval develop- 
ment. As JONES (1963) and YONGE (1969) considered typ- 
ical of carditids, the larvae were numerous (approximately 
100 individuals in Cardita aviculina), contained in the in- 
terlamellar space of both the right and left inner demi- 
branchs, and were all at the same stage of development. 
The larvae were non-shelled, circular, undifferentiated, 
with an outer membrane and a very faint inner membrane. 
The diameter of the larvae ranged from 0.20 mm to 0.22 
mm, larger than larvae of Glans carpenter (0.12 mm), but 
smaller than those of Cyclocardia ventricosa (0.50 to 0.58 
mm). 

Coan (1977) speculated that brooding may hinder gene 
flow, and therefore lead to considerable morphologic vari- 
ation between populations. Indeed, LAMy (1922) recog- 
nized multiple varieties of many widespread species of 
carditids, including four varieties of Cardita aviculina (C. 
aviculina occurs throughout the Indo-Pacific [Lamy, 1922], 
Hawaii [Kay, 1979], and the eastern Pacific [SHASKY, 
1986]). However, the varieties are not allopatric, because 
the geographic distributions of the varieties are patchy and 
overlapping. 

DALL (1903) suggested that all members of the Car- 
ditidae may brood their larvae, and YONGE (1969) and 
COAN (1977) also considered this possibility. STRATHMANN 
(1985) has argued that taxa with lecithotrophy (non-feed- 
ing larvae, which would include those which are brooded) 
are derived from taxa with planktotrophy (feeding larvae), 
but rarely the reverse. Brooding may then be considered 
either (1) primitive for the Carditidae, or (2) having in- 
dependently evolved several times. Since planktotrophy is 
as yet unknown in the Carditidae, alternative (1) is the 
more likely scenario. However, this question cannot be 
fully resolved until more species of Carditidae are studied 
and the group is examined phylogenetically. 


Acknowledgments 


G. M. Davis lent me the material to study. P. H. Scott 
and E. V. Coan resolved a taxonomic question regarding 
Glans carpenteri. E. V. Coan, M. LaBarbera, D. Jablonski, 
and an anonymous reviewer provided helpful comments. 


Literature Cited 


Coan, E. V. 1977. Preliminary review of the northwest Amer- 
ican Carditidae. The Veliger 19:375-386. 

Dat, W. H. 1903. Synopsis of the Carditacea and of the 
American species. Proceedings of the Academy of Natural 
Sciences of Philadelphia 54:696-716. 


Notes, Information & News 


Page 95 


Heasiip, W. G. 1968. Cenozoic evolution of the alticostate 
venericards in gulf and east coastal North America. Palaeon- 
tographica Americana 6:55-135. 

HeEasuip, W. G. 1969. Sexual dimorphism in bivalves. Pp. 60- 
75. In: G. E. G. Westermann (ed.), Sexual Dimorphism in 
Fossil Metazoa and Taxonomic Implications. E. Schweiz- 
erbart’sche Verlagsbuchhandlung (Nagele u. Obermuller): 
Stuttgart, Germany. 

JABLONSKI, D. & R. A. Lutz. 1980. Larval shell morphology: 
ecological and paleontological applications. Pp. 323-377. In: 
D. GC. Rhoads & R. A. Lutz (eds.), Skeletal Growth of 
Aquatic Organisms. Plenum Press: New York, New York. 

JABLONSKI, D. & R. A. Lutz. 1983. Larval ecology of marine 
benthic invertebrates: paleobiological implications. Biologi- 
cal Reviews 58:21-89. 

Jones, G. F. 1963. Brood protection in three southern Cali- 
fornia species of the pelecypod Cardita. The Wasmann Jour- 
nal of Biology 21:141-148. 

Kay, E. A. 1979. Hawaiian Marine Shells. Reef and Shore 
Fauna of Hawaii. Section 4: Mollusca. Bernice P. Bishop 
Museum Special Publication 64(4). Bishop Museum Press: 
Honolulu. 653 pp. 

Lamy, E. 1922. Revision des Carditacea vivants du Museum 
National d’Histoire Naturelle de Paris. Journal de Con- 
chyliologie 66:218-276. 

SHASKY, D. R. 1986. Update on mollusks with Indo-Pacific 
faunal affinities in the tropical eastern Pacific 4. The Festivus 
18:3-5. 

STRATHMANN, R. R. 1985. Feeding and non-feeding larval 
development and life-history evolution in marine inverte- 
brates. Annual Review of Ecology and Systematics 16:339- 
361. 

YONGE, C. M. 1969. Functional morphology and evolution 
within the Carditacea (Bivalvia). Proceedings of the Mal- 
acological Society of London 38:493-527. 


In Situ Spawning Behavior of an Alaskan 
Population of Pinto Abalone, 
Haliotis kamtschatkana Jonas, 1845 
by 
Michael S. Stekoll 
School of Education, Liberal Arts and Sciences, 
University of Alaska Southeast, 

11120 Glacier Highway, 

Juneau, Alaska 99801, USA 
and 
Thomas C. Shirley 
Juneau Center for Fisheries and Ocean Science, 
University of Alaska Fairbanks, 

11120 Glacier Highway, 

Juneau, Alaska 99801, USA 


Introduction 


The pinto abalone (Haliotis kamtschatkana Jonas, 1845) 
supports a small commercial fishery in southeastern Alas- 
ka, but few studies have addressed its biology in the Alas- 
kan part of its range (LIVINGSTONE, 1952; PAUL et al., 
1977; PAUL & PAUL, 1981; STANDLEY, 1987). In British 
Columbia the species supported a much larger fishery until 
its closure in 1990 and has been the subject of many studies 


(BREEN, 1980, 1986; BREEN & ADKINS, 1979, 1980; 
QUAYLE, 1962, 1971; SLOAN & BREEN, 1988). 

Knowledge of the reproductive biology of the species is 
important for management, as fishery openings might be 
timed to permit reproduction prior to harvest. No clearly 
defined reproductive cycle was evident in gonadal sections 
from British Columbia specimens; however, spontaneous 
spawning by pinto abalone in laboratory cultures was ob- 
served (QUAYLE, 1971). An in situ spawning of pinto ab- 
alone was observed in mid-July in the Queen Charlotte 
Islands; but, because approximately 500 abalone had been 
handled and aerially exposed while being tagged with plas- 
tic spaghetti tags before their return to the water, a strong 
possibility existed that handling had induced the spawning 
(BREEN & ADKINS, 1980). STANDLEY (1987) extensively 
studied the reproductive biology of pinto abalone from 
Sitka Sound; she observed spontaneous laboratory spawn- 
ing of pinto abalone (primarily in early summer) and was 
able to induce spawning by a variety of methods, but did 
not observe im situ spawning. The lack of observations of 
in situ spawning of pinto abalone is not unusual, as ob- 
servations of any species of abalone spawning are rare 
(Haun, 1989). 


Observations 


Observations of spawning abalone were made with the aid 
of SCUBA near the mouth of Whiting Harbor, Sitka, Alaska 
(57°03'15”N, 135°22'22”W) at 1730 hr on 30 July 1991. 
Most of the abalone observed spawning were males at 
between 3 and 5 m depth. The weather was overcast, with 
calm seas and little wind; air temperature was 13.9°C. The 
water column had little temperature or salinity stratifi- 
cation; temperature varied by less than 1°C and salinity 
varied by less than 1 ppt between the surface and 5 m 
depth, and only slightly more variation was present to 10 
m depth (Table 1). Observations were made approxi- 
mately one hour after high tide; currents were minimal 
and gametes slowly dissipated (Figure 1). Tidal ranges 
were intermediate between spring and neap tides. The 
spawning population was videotaped; 35-mm underwater 
cameras were also used to document the event. 

Red sea urchins, Strongylocentrotus franciscanus (A. Ag- 
assiz, 1863), and topsnails (Calliostoma sp.) were the most 
common macrofauna other than abalone, but the sunflower 
star, Pycnopodia helianthoides (Brandt, 1835), and kelp 
greenling, Hexagrammos decagrammus (Pallas, 1810), were 
present. 


Discussion 


It is unlikely that diver activities triggered spawning, be- 
cause spawning was in progress at first observation and 
occurred prior to any handling. MOTTET (1978) and HAHN 
(1989) reviewed exposure and rapid temperature changes 
as natural spawning stimuli for a variety of abalone species. 
BREEN & ADKINS (1980) suggested that tidal temperature 
rhythm might be a spawning stimulus for pinto abalone, 


Page 96 


The Veliger, Vol. 36, No. 1 


Table 1 


Temperature (°C) and salinity (ppt) by depth at the time 
of spawning observations of pinto abalone, Haliotis kam- 
tschatkana, in Sitka Sound, Alaska, on 30 July 1991. 


Depth Temperature Salinity 
(m) CC) (ppt) 
0.2 13.22 29.99 
1 13 17 30.01 
2 13.13 30.01 
3 13.05 30.04 
4 12.76 30.20 
5 12.64 30.30 
6 12.57 30.33 
7 12.13 30.76 
8 12.06 30.79 
9 12.00 30.83 
10 11.86 30.93 


explaining the spatial and temporal variability that has 
been reported (QUAYLE, 1971). These suggestions offer 
little explanation for our spawning observations. The pinto 
abalone observed in Sitka Sound were below the depth of 


tidal exposure, the water column had little temperature 
stratification, and spawning was observed shortly after 
high tide, when the abalone would have been exposed to 
the smallest temperature variation. 

Pinto abalone are not unusual in the variability that has 
been reported for their gonadal maturation and spawning 
periods. A wide variability in spawning times has been 
reported for abalone both within and between species 
(HAHN, 1989; MoTTET, 1978). Black abalone, Haliotis 
cracherodu Leach, 1814, populations only a few kilometers 
apart in California had different spawning times (WEBBER 
& GIESE, 1969). Similarly, H. rubra at different locations 
in Australia had vastly different spawning periods, and in 
different seasons (SHEPHERD & Laws, 1974). 

The spatial extent of abalone spawning on the day of 
our observations is unknown; however, all abalone ob- 
served at the site were spawning, including the smallest 
individuals. The distribution of abalone was patchy; areas 
of high density were interspersed with areas containing no 
abalone. The implication from the observed distributions 
is that the abalone formed many, small spawning aggre- 
gations. 

The pinto abalone appeared to be climbing as high above 


Figure 1 


Spawning pinto abalone, Haliotis kamtschatkana, on stipe of Pleurophycus sp. A red sea urchin is in the foreground 
and other abalone are visible in the background (photograph by M. Ridgway). 


Notes, Information & News 


Page 97 


the bottom as possible. Most abalone were on the stipes 
of Pleurophycus sp. and Laminaria sp. (although some were 
observed on blades of Costaria sp. and Macrocystis sp.), 
with many abalone stacked on top of each other, up to five 
individuals high, with the uppermost individual being up 
to 1-2 m above the substrate. Interestingly, only males 
were observed in stacks; however, since the sexes were 
identified primarily by their gametes, females could have 
been missed. Upward vertical movements of abalone prior 
to spawning (primarily in laboratory culture) have been 
reported for numerous species (see reviews by MOTTET, 
1978; HAHN, 1989), including pinto abalone (QUAYLE, 
1971; BREEN & ADKINS, 1980). 

BREEN & ADKINS (1980) suggested the vertical move- 
ments might be a mechanism for concentrating the adults, 
or alternatively, strategies for releasing gametes into the 
warmest water possible or for exposing eggs to the greatest 
amount of sperm before settling to the bottom. They argued 
that the adult concentrations might have strong adaptive 
roles, and that decreases in local density due to overhar- 
vesting might have a pronounced influence on recruitment 
success. LEVITAN et al. (1992) reported that the distribution 
and abundance of spawning organisms can have a pro- 
found influence on reproductive success and quantified the 
significance of spawning concentrations. 

Our observations constitute the first published report of 
in situ spawning of pinto abalone in Alaskan waters, con- 
firm the observations of BREEN & ADKINS (1980) made in 
British Columbian waters, and extend the documented 
spawning time of pinto abalone until late July. 


Acknowledgments 


We thank M. Ridgway, who made the initial spawning 
observations, and P. Else for their assistance with under- 
water photography and data collection. This project was 
funded by the National Oceanic and Atmospheric Admin- 
istration, U.S. Department of Commerce, Washington, 
D.C., through grant Nos. NA87AA-D-SG065 and 
NA16RG0167-01 to the National Coastal Resources Re- 
search and Development Institute, Portland, Oregon. Oth- 
er funding was provided by the Japan Overseas Fisheries 
Cooperation Foundation (Japan OFCF) and the Alaska 
Department of Commerce and Economic Development. 


Literature Cited 


BREEN, P. A. 1980. Measuring fishing intensity and annual 
production in the abalone fishery of British Columbia. Ca- 
nadian Technical Reports, Fisheries and Aquatic Sciences 
947:49 pp. 


BREEN, P. A. 1986. Management of the British Columbia 
fishery for northern abalone (Haliotis kamtschatkana). Pp. 
300-312. In: G. S. Jamieson & N. Bourne (eds.), North 
Pacific Workshop on Stock Assessment and Management of 
Invertebrates. Canadian Special Publications on Fisheries 
and Aquatic Sciences 92. 

BREEN, P. A. & B. E. ADKINS. 1979. A survey of abalone 
populations on the east coast of the Queen Charlotte Islands, 
August 1978. Fishery Marine Service Manuscript Reports 
1490:1-125. 

BREEN, P. A. & B. E. ADKINS. 1980. Spawning in a British 
Columbia population of northern abalone, Haliotis kam- 
tschatkana. The Veliger 23:177-179. 

HAHN, K. O. 1989. Gonad reproductive cycles. Pp. 13-39. In: 
K. O. Hahn (ed.) Handbook of Culture of Abalone and 
Other Marine Gastropods. CRC Press: Boca Raton, Florida. 

LEvITAN, D. R., M. A. SEWALL & F.-S. Cuta. 1992. How 
distribution and abundance influence fertilization success in 
the sea urchin Strongylocentrotus franciscanus. Ecology 73(1): 
248-254. 

LIVINGSTONE, R., JR. 1952. Preliminary investigation of the 
southeastern Alaska abalone (Haliotis kamtschatkana). Part 
I—exploratory diving. Commercial Fisheries Review 14:8- 
16. 

MotteT, M. G. 1978. A review of the fishery biology of 
abalones. Washington State Department of Fisheries Tech- 
nical Report 37:1-87. 

Pau, A. J., J. M. Pau, D. Hoop & R. A. NEvE. 1977. 
Observations on food preferences, daily ration requirements 
and growth of Haliotis kamtschatkana Jonas in captivity. The 
Veliger 19:303-309. 

PAUL, A. J. & J. M. PauL. 1981. Temperature and growth of 
maturing Halvotis kamtschatkana Jonas. The Veliger 23:321- 
324. 

QuaYLE, D. B. 1962. Abalones of British Columbia. Fisheries 
Research Board Canada Progress Report of Pacific Coast 
Stations 114:9-12. 

QuaYLE, D. B. 1971. Growth, morphometry and breeding in 
the British Columbia abalone (Haliotis kamtschatkana Jonas). 
Fisheries Research Board Canada Technical Report 279:1- 
84. 

SHEPHERD, S. A. & H. M. Laws. 1974. Studies on southern 
Australian abalone (genus //aliotis). II. Reproduction of five 
species. Australian Journal of Marine and Freshwater Re- 
search 25(1):49-62. 

SLOAN, N. A. & P. A. BREEN. 1988. Northern abalone, Haliotis 
kamtschatkana, in British Columbia: fisheries and synopsis 
of life history information. Canadian Special Publications 
on Fisheries and Aquatic Sciences 103:1-46. 

STANDLEY, C. S. 1987. Temperature and salinity effects on 
gamete viability and early development of pinto abalone, red 
sea urchins and green sea urchins. Master’s Thesis. Uni- 
versity of Alaska-Juneau, Juneau. 90 pp. 

WEBBER, H. H. & A. C. GIESE. 1969. Reproductive cycle and 
gametogenesis in the black abalone Haliotis cracherodi (Gas- 
tropoda: Prosobranchiata). Marine Biology 4(2):152-159. 


The Veliger 36(1):98 (January 4, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


BOOKS, PERIODICALS & PAMPHLETS 


The Encyclopedia of Seashells 


by GARY ROSENBERG. 1992. Michael Friedman Publishing 
Group, Inc., New York. 224 pp. Hardcover $20. North 
American distribution through B. F. Dalton and Barnes 
and Noble bookstores. 


At first glance, this attractive mass-marketed volume 
has all the trappings of one more coffee-table shell book. 
The dust jacket is one of those arrangements of colorful 
shells artistically deployed in orientations and at scales 
that disturb the professional eye. The frontispiece is a 
photographic jumble of sea treasures (with as many echi- 
noderms, cnidarians, and barnacles as mollusks, all seem- 
ingly nestled into a bed of soapsuds), and the shell on the 
page facing the table of contents is propped shamelessly 
in the swash in a seductive, pink-lipped, apertural display. 

Then the author assumes control, and the tone changes. 
The page facing the preface is a reproduction of a hand- 
colored plate from Chenu’s //lustrations Conchyliologiques, 
and by page 8, voila, a full-page cladogram! In the disguise 
of a coffee-table book, Gary Rosenberg has produced an 
affordable scholarly reference that fills an empty niche. It 
offers a self-starting education in molluscan taxonomic 
diversity that begins with the shell, while providing the 
reader with some basic anatomical information, a basic 
technical glossary, and a geographical index to shell iden- 
tification guides. Most importantly, it provides a bibliog- 
raphy of nearly 400 references to authoritative primary 
literature for the major families of shelled marine mollusks. 

The author has achieved a scholarly goal in spite of 
what sounded like an intellectually vacuous contract charge 
to produce a picture book of pretty shells. Working within 
the constraint of selecting 250 species (one color illustration 
and 200 words each), Gary Rosenberg arrived at the clever 
subterfuge of choosing each species to represent a different 
family, or in some instances subfamily. The color photo- 
graphs (mostly the work of the author) are outstanding, 
and in addition to a brief account of each illustrated species 
there is an informative summary of the family. In the case 
of two of the hydrothermal vent taxa (Neomphalus fretterae 
and Calyptogena magnifica) Rosenberg has photographed 
paratype material, although specimen data and reposito- 
ries are beyond the limits of the subterfuge. 

In spite of the absence of catalog numbers on any of the 
photographed specimens, the chapter on shell collecting 
presents the amateur collector or student with unusually 
rigorous instructions and challenges to data collection and 
data management. This includes a section of advice on 
information fields and database programs for curating per- 
sonal shell collections with a home computer. 

If this were intended as a technical publication or text- 
book, I would be tempted to critique specifics of content 
and omissions; but that is not appropriate here. What is 


important is the appearance of a unique reference work 
that presents molluscan diversity systematically to the non- 
professional as an intellectually challenging subject and 
that speaks of natural history in the best sense of the 
tradition. 


Carole S. Hickman 


Eocene Mollusca from the Vicinity of 
McCulloch’s Bridge, Waihao River, 
South Canterbury, New Zealand: 
Paleoecology and Systematics 


by PHILLIP A. MAXWELL. 1992. New Zealand Geological 
Survey Paleontological Bulletin 65. 280 pp.; 30 plates. 
Paperback $70. Publications Officer, DSIR Geology & 
Geophysics, P.O. Box 30 368, Lower Hutt, New Zealand. 
FAX (04) 5695-016. 


This faunal monograph continues in the exemplary 
modern tradition set by New Zealand paleontologists. It 
provides the first comprehensive documentation of one of 
the most spectacular Eocene molluscan faunas in the 
Southern Hemisphere, recording 250 species. The mono- 
graph introduces 10 new generic names and 89 new species 
(18 bivalves, 64 gastropods, and 7 scaphopods). There are 
42 new combinations; and the new taxa, new combinations, 
and new synonymies are conveniently summarized in an 
appendix. Separate sections provide detailed analysis of 
the composition of the fauna, family by family, and the 
paleoecology. The plates (which contain 438 photographs) 
are of high quality. Two distinctive faunules, both from 
outer shelf to upper bathyal tuff beds, dominate the mono- 
graph and will play a major role in any reevaluation of 
the evolution of Eocene offshore faunas. 

The mollusks of classic McCulloch’s bridge locality have 
been collected and partially described over a period of 125 
years. This long-awaited and meticulously updated pub- 
lication is Phil Maxwell’s Ph.D. thesis, prepared approx- 
imately 20 years ago. It is indeed fortunate that this work 
has made it to publication in spite of the budgetary crises 
and the changing complexion of government science in 
New Zealand that has eliminated Maxwell’s position and 
transformed the New Zealand Geological Survey first into 
the “Department of Scientific and Industrial Research: 
Geology and Geophysics,” and more recently into the “‘In- 
stitute of Geological and Nuclear Sciences Limited” (a 
government “science company’”’). 


Carole S. Hickman 


Information for Contributors 


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Cate, J. M. 1962. On the identifications of five Pacific Mitra. The Veliger 4:132-134. 


b) Books 


Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London. 
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CONTENTS — Continued 


First report of the ovulid gastropod Sulcocypraea mathewsonu (Gabb, 1869) from 
the Eocene of Washington and Oregon and an additional report from 
California 

RICHARD, LE. SQUIRES AND) LINDSEY? LS GROVES 5 eee 


New records for ranellid gastropods in the western Atlantic (Ranellidae: Cy- 
matiinae) 
BETTY JEAN PIECH 


NOTES, INFORMATION & NEWS 


Predation by Latiaxis oldroydi (Gastropoda: Coralliophilidae) on Corynactis 
californica (Anthozoa: Corallimorphidae) 
Mary K. WICKSTEN AND ROBERT I: WRIGHT 2-2-7550) ee 


Invasion of the south ‘Texas coast by the edible brown mussel Perna perna 
(Linnaeus, 1758) 
DAvip W. Hicks AND JOHN W. qiUNNEEL, JR] G2. 0-902)  eeee 


Brooding of larvae in Cardita aviculina Lamarck, 1819 (Bivalvia: Carditidae) 
JAY A; SCHNEIDER a5)! 5 AoGo5 Ghai ee oe ec eee 


In situ spawning behavior of an Alaskan population of pinto abalone, Halvotis 
kamtschatkana Jonas, 1845 
MICHAELS. STEKOLE AND: THOMAS; C: SHIRLEY 9227224. 22 45) ee 


BOOKS; PERIODICALS & PAMPHEEUS: 350 he eee 


7 


) | 
1, THE 


‘VELIGER 


; 


_ ISSN 0042-3211 


A Quarterly published by 
CALIFORNIA MALACOZOOLOGICAL SOCIETY, nel? 
Berkeley, California 

R. Stohler, Founding Editor 


Volume 36 


CONTENTS 


Population structure of two common species of ascoglossan (= sacoglossan) opis- 
thobranchs on the central coast of Oregon, USA 
CVINGETAG DSSPROWBRIDGHM Sans ih ee ca ca eminence es Al noes | 99 


Fine structure of the three cell types found in the digestive gland of Elysia viridis 
(Opisthobranchia: Sacoglossa) 
RCE GINA GIRUEB ET ere te ese any A Ge he tare Gh ee aye ates Ge ees 107 


Behavioral interactions among nudibranchs inhabiting colonies of the hydroid 
Obelia geniculata 
NPAT ERG) SaIOAMIBER Mas Wee eimi ae rota nay hiya a etek e a neh are des Le M5 


Redescription and taxonomic reappraisal of the tropical Indo-Pacific nudibranch 
Straus nucleola (Pease, 1860) (Anthobranchia: Doridoidea: Dorididae) 
GINTANNE) P| BRODIE AND: RICHARD Ge WILLAN 2.25. 5202-2 ese. eee: 124 


Polygyrid land snails, Vespericola (Gastropoda: Pulmonata), 1. Species and pop- 
ulations formerly referred to Vespericola columbianus (Lea) in California 
BARRYSROMHOANDEV ALTER B-OMIEEER a5) 23424. Ye see 134 


Slugs of Portugal. III. Revision of the genus Geomalacus Allman, 1843 (Gas- 
tropoda: Pulmonata: Arionidae) 
T. RODRIGUEZ, P. ONDINA, A. OUTEIRO, AND J. CASTILLEJO ........... 145 


The taxonomic status of Buccinanops d’Orbigny, 1841 (Gastropoda: Nassariidae) 
SUID OMASHORIN OW here ee ene) caren rere oe oat ele ee Me eracs oe 160 


CONTENTS — Continued 


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THE VELIGER 


Scope of the journal 
The Veliger is open to original papers pertaining to any problem concerned with mollusks. 

This is meant to make facilities available for publication of original articles from a 
wide field of endeavor. Papers dealing with anatomical, cytological, distributional, eco- 
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The Veliger 36(2):99-106 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Population Structure of Two Common Species of 


Ascoglossan (= Sacoglossan) Opisthobranchs on 
the Central Coast of Oregon, USA 


by 


CYNTHIA D. TROWBRIDGE! 


Department of Biology, Syracuse University, Syracuse, New York 13244, USA 


Abstract. 


The herbivorous ascoglossan opisthobranch fauna in the N.E. Pacific has been extensively 


studied in terms of species diversity, geographic range, seasonality, and host-plant associations. Yet, 
basic demographic information is lacking for most of the local species. To fill this gap, two common 
species of ascoglossans were examined along the central coast of Oregon, USA: the large, conspicuous 
Aplysiopsis enteromorphae (Cockerell & Eliot, 1905) and the small, cryptic Alderia modesta (Loven, 1844). 
Three aspects of demography were quantified: (1) population structure and size range, (2) length-weight 
relationships, and (3) size-specific egg mass deposition. During the summer of 1990, Aplysiopsis enter- 
omorphae collected from high intertidal, saline pools at Strawberry Hill and Neptune Beach state parks, 
Oregon varied in size from 4 to 277 mg (wet weight). These values corresponded to body lengths of 
~5 to 20 mm. Most Aplysiopsis enteromorphae deposited egg masses in the laboratory, and egg mass 
weight was unrelated to ascoglossan body size. Thus, in contrast to many other opisthobranchs, there 
was no apparent fecundity advantage of large size. In June 1990, Alderia modesta collected from high 
intertidal algal mats in Yaquina Bay, Oregon ranged in size from 0.4 to 13.3 mg (wet weight). Most 
individuals were <6 mm in length. The proportion of ascoglossans depositing egg masses was size 
specific: Alderia modesta <2 mg commonly did not produce egg masses whereas individuals >3 mg 
almost always deposited eggs. The minimum size of egg deposition was extremely small for both species: 
<4 mg in Aplysiopsis enteromorphae and <0.4 mg in Alderia modesta. Therefore, the majority of indi- 
viduals in populations of both species were reproductively competent. Early, continuous reproduction 
may be a mechanism for some ascoglossans to ensure production of offspring under unpredictable 


conditions. 


INTRODUCTION 


Ascoglossan (= sacoglossan) opisthobranchs are a common, 
though often overlooked, group of mollusks because of their 
generally small size, often cryptic coloration, and patchy 
distribution (MILLEN, 1980). Although the biology of the 
ascoglossan fauna has been studied in detail for many 
geographic regions (e.g., N.W. Atlantic, Caribbean, N.E. 
Atlantic, Mediterranean), there is a comparative paucity 
of basic information on species in the N.E. Pacific. Even 
when species appear cosmopolitan, extrapolations from 
different geographic regions may not necessarily be reliable 


' Present address: Leigh Marine Laboratory, University of 
Auckland, P.O. Box 349, Warkworth, New Zealand. 


because of different (1) abiotic factors (e.g., tidal patterns, 
water temperature, upwelling regimes) and (2) biotic fac- 
tors (e.g., predators, competitors, algal host species). Re- 
gional and local information on ascoglossan populations 
is, therefore, merited. 

Four species of N.E. Pacific ascoglossans are common: 
Placida dendritica (Alder & Hancock, 1843), Elysia hedg- 
pethi (Marcus, 1961), Aplysiopsis enteromorphae (Cockerell 
& Eliot, 1905), and Alderia modesta (Lovén, 1844). The 
extent of ranges of these species and other, less common 
ascoglossans has been examined by many workers (LANCE, 
1961, 1966; Marcus, 1961; STEINBERG, 1963; Mac- 
FARLAND, 1966; SPHON & LANCE, 1968; ROLLER & LONG, 
1969; GOSLINER & WILLIAMS, 1970; SPHON, 1971; WIL- 
LIAMS & GOSLINER, 1973; LAMBERT, 1976; MILLEN, 1980, 
1989; GODDARD, 1984; FOSTER, 1987; BEHRENS, 1991). 


Page 100 


A. Marine, Rocky Shore 


Seepage Pool 
(Enteromorpha) 


{ 


Saline Pool 
(Cladophora & 


Barnacles | Chaetomorpha) 


Rockweeds 


B. Estuary 


High Marsh 
4, (grasses) 
II 


~ uy Vaucheria Mat 
(pickleweed) 


Mud Flat 
Figure 1 


Profile of shores illustrating location of ascoglossan habitats. A. 
High intertidal, open-coast pools containing filamentous green 
algae (Cladophora, Chaetomorpha) with the ascoglossan Aplysiop- 
sis enteromorphae. B. High intertidal, estuarine algal mats (Vauch- 
eria) with the ascoglossan Alderia modesta. 


In contrast, aspects of ascoglossan population ecology have 
received comparatively little attention. Detailed informa- 
tion is known about the population structure and dynamics 
of P. dendritica on the Oregon coast (TROWBRIDGE, 199 1a, 
b, 1992a, b). Furthermore, more limited data on feeding, 
egg masses, and veligers exist (HAND & STEINBERG, 1955; 
Gonor, 1961; GREENE, 1968). The objective of the present 
study was to provide descriptive information on the pop- 
ulation structure of two common species: Aplysiopsis en- 
teromorphae and Alderia modesta. 


NATURAL HISTORY 


Aplysiopsis enteromorphae (reported primarily as A. smithi 
before BEHRENS (1991)) has a limited geographic distri- 
bution, inhabiting N.E. Pacific shores from Alaska to the 
Gulf of California (LANCE, 1961; ROLLER & LONG, 1969; 
GOSLINER & WILLIAMS, 1970; MILLEN, 1980, 1989; BEH- 
RENS, 1991). The opisthobranch has a disjunct local dis- 
tribution, occurring (1) in high intertidal, open-coast pools 
on filamentous green algae and (2) in bays and estuaries 
on green algal mats (GONOR, 1961; STEINBERG, 1963; 
GREENE, 1968; GOSLINER & WILLIAMS, 1970; WILLIAMS 
& GOSLINER, 1973; GODDARD, 1984; TROWBRIDGE, in 
press). Although the conspicuous ascoglossan regularly oc- 
curs in both habitats, its low density makes A. enteromor- 


The Veliger, Vol. 36, No. 2 


phae a predictably sparse species. The ascoglossan occurs 
on the shore from April or May to September in Wash- 
ington and Oregon (GoNoR, 1961; GODDARD, 1984; 
TROWBRIDGE, in press) and from January to June in Cal- 
ifornia (LANCE, 1961). Individuals of the species attain 
lengths of 2 to 3 cm (TROWBRIDGE, in press). 

Alderia modesta inhabits temperate and boreal estuaries 
throughout the Northern Hemisphere (HARTOG & 
SWENNEN, 1952; HAND, 1955; HAND & STEINBERG, 1955; 
HarToc, 1958, 1959; STEINBERG, 1963; BLEAKNEY & 
BAILEY, 1967; CLARK, 1975; THOMPSON, 1976; MILLEN, 
1980, 1989; VADER, 1981; ROGINSKAJA, 1984). The as- 
coglossan occurs in association with the high intertidal, 
mat-forming, yellow-green alga Vaucheria sp. that grows 
within and directly downshore from salt marsh vegetation 
such as pickleweed (Salicornia) (HAND & STEINBERG, 1955; 
HarTOG, 1959; STEINBERG, 1963; VADER, 1981). Alderia 
modesta often forms high-density populations, ranging from 
tens to thousands of animals per square meter (HARTOG, 
1959; SEELEMANN, 1967; VADER, 1981; TROWBRIDGE, un- 
published data). Larvae of A. modesta settle, metamor- 
phose, and recruit to the algal mats during spring, summer, 
and fall in most Atlantic localities (HARTOG, 1959; VADER, 
1981). My observations of juveniles (1 to 2 mm long) in 
winter on Oregon mudflats indicate that the herbivore may 
have broader seasonality in the N.E. Pacific. Alderia mo- 
desta grows to sexual maturity in ~10 days after meta- 
morphosis (SEELEMANN, 1967) and attains maximum 
lengths of 5 to 16 mm, depending upon locality (ENGEL 
et al., 1940; HAND & STEINBERG, 1955; HarToc, 1959; 
BLEAKNEY & BAILEY, 1967; THOMPSON, 1976). 

The two ascoglossan species, therefore, exhibit a number 
of striking differences including breadth of geographic 
range, extent of habitat specificity, population density, phe- 
nology, and body size. In this study, three aspects of as- 
coglossan population structure were quantified: (1) size- 
frequency distribution and size range, (2) length-weight 
relationship, and (3) size-specific egg mass production. 


MATERIALS ano METHODS 
Collection Locations 


Aplysiopsis enteromorphae was collected from filamen- 
tous green algae in high intertidal, saline pools at Straw- 
berry Hill and Neptune Beach state parks (44°15’N, 
124°7'W) on the central coast of Oregon, USA. Pools ranged 
in tidal level from the upper end of the acorn barnacle 
zone (primarily Balanus glandula) to the upper end of the 
rockweed zone (Pelvetiopsis limitata) (Figure 1A). Alderia 
modesta was collected from mats of the yellow-green alga 
Vaucheria sp. on the south shore of Yaquina Bay, Oregon 
(44937'N, 124°3'W). The algal mats occurred directly 
downshore from salt marshes (Figure 1B), particularly 
low marshes composed of pickleweed (Salicornia virginica). 
Ascoglossans were brought back to the Hatfield Marine 
Science Center in Newport, Oregon for measurement. 


C. D. Trowbridge, 1993 


Page 101 


Aplysiopsis enteromorphae 


Viscmegei leas =| 
eey 23 (n=91) | 

June 11 (n=135) | 
a 


| 


7 F T T 


n BY 4 - Rom Fin FF ms 
= O Fo ihe Sie Sis TiS Ge Ge SE 
a 0- 10- 20- 30- 40- 50- 60- 70- 80- 90- =100 
~”A 
2 40 
oD | June 22 (n=187) | 
io) 
(5) 
A 
< 
me 
io) 
& 
30+ ZZ July 23 (n=60) 4 
L : Aug. 8 (n=88) 
20 : a? 1 
10+ z | A 
i be 
0 gi Hl E; 5 4 4 4 
30- 40- 50- 60- 70- 80- 90- 2100 


0- 10- 20- 


Wet Weight (mg) 
Figure 2 


Size-frequency distributions of Aplysiopsis enteromorphae in high 
intertidal pools at Strawberry Hill and Neptune Beach state 
parks, Oregon at two-week intervals in 1990. Data were pooled 
from the two sites. Sample sizes indicate the number of individuals 
weighed for each collection. 


Procedures 


From May to August 1990, Aplysiopsis enteromorphae 
was collected every two weeks from all available pools at 
the two sites. Measurements of ascoglossan size were based 
primarily on wet weight because it was faster to quantify 
and more repeatable than body length for unanaesthetized 
animals. Each individual was gently blotted and weighed 
to the nearest milligram. More accurate estimates could 
not be reliably made for A. enteromorphae because of (1) 
copious secretion of mucus and viscous white fluid and (2) 
autotomy of cerata when disturbed. In the late July sample, 
the body length of A. enteromorphae was measured to the 
nearest millimeter using a dissecting microscope with an 
ocular micrometer. 

In June 1990, Alderia modesta was collected from three 
randomly placed 0.25-m? quadrats on the south shore of 
Yaquina Bay, Oregon. Because of the high disturbance 
threshold of A. modesta, individuals could be weighed with 
more accuracy, to the nearest 0.01 mg. In late July, another 
batch of ascoglossans was collected for a length-weight 
comparison. Body length was measured, as before with an 
ocular micrometer, to the nearest millimeter. 

The size-specific egg mass production of each species 


Alderia modesta 


% of Ascoglossans 


0 1 2 3 4 5 6 7 8 9 10 41 12 13 14 


Wet Weight (mg) 
Figure 3 


Size-frequency distribution of Alderia modesta on high intertidal 
Vaucheria mats in Yaquina Bay, Oregon in June 1990. Data 
were pooled from three randomly selected 0.25-m? quadrats. 
Sample size indicates the number of individuals weighed. 


was estimated in the laboratory. Individual pre-weighed 
ascoglossans were placed in separate plastic petri dishes 
with fresh seawater. Petri dishes were set in a constant 
temperature room at 11°C, and the seawater was changed 
daily. The temperature was comparable to sea surface 
temperature in the field. After three days, the presence or 
absence of egg masses in each petri dish was noted. Egg 
masses of Aplysiopsis enteromorphae were gently blotted 
and weighed to the nearest milligram (wet weight). Egg 
masses were then dried for 24 hr at 50°C and then re- 
weighed (dry weight). Because of the small size of egg 
masses of Alderia modesta, complementary data on wet and 
dry weight were not collected: most values were below the 
level of detection on the available balance (0.01 mg). 


RESULTS 
Size Structure 


From May to August 1990, Aplysiopsis enteromorphae 
varied in size from 4 to 277 mg (wet weight) with a range 
of sizes occurring in all six biweekly samples (Figure 2). 
In early May, A. enteromorphae was not found in the pools. 
The sample on 23 May, therefore, was comprised of an- 
imals <2 weeks old. Either adult ascoglossans had mi- 
grated into the pools, perhaps from subtidal algae, or in- 
dividuals had grown up to over 100 mg in the intervening 
period. Because virtually all the ascoglossans were removed 
from every available pool encountered at Strawberry Hill 
and Neptune Beach, the size-frequency distributions re- 
flected primarily settlement and/or growth within each 
2-week period. The distributions did vary significantly 
among sampling periods (G-test, G = 199.0, 20 df, n = 
740, P < 0.001). Samples on 11 and 22 June had a greater 


Page 102 The Veliger, Vol. 36, No. 2 


A. Aplysiropsis B. A/deria 


250 
% ® 
sp 200 Neptune ® a 
& & 
= 150 Beach Strawberry z 
ce} Hill c: 
o r ) oO 
= 100 Ory, Es 
rs) e 8 “a o 
Es mete. Es 
50 e 44,8 
ogtal’: 
0 
5 10 15 20 25 


Body Length (mm) 
Figure 4 


Length-weight relationships for Aplysiopsis enteromorphae (A) and Alderia modesta (B) in July 1990. Collection sites 
are indicated. Vertical dashed line (B) indicates approximate maximum size of Alderia modesta in Yaquina Bay, 


Oregon. 
A. Egg Masses B. Fecundity C. Precision 
© Absent 
Present 
100 
r=0.987 
80 i ° n=72 
~ / rg=0.071 P<0.001 
q £ eta ps 
bs ng i n=72 = 
on 08 e) P>0.50 mal 
eo o = 
8 z i. 
S240 E 
oO 
‘ a 3 
ea) 
20 


= 

= = 

= = 
= = & 


0 bo = S 
Body Weight (me) Body Weight (mg) Dry Weight (mg) 
Figure 5 


Egg mass production of Aplysiopsis enteromorphae in the laboratory (3 days, 11°C). A. Percentage of ascoglossans 
producing egg masses (n denotes number of individuals measured). B. Scatter plot of egg mass and ascoglossan 
body weight. Vertical dashed line indicates the minimum size of egg mass production; dotted line indicates the 1:1 
ratio of egg mass to body weight. C. Correlation of wet and dry weight of 72 A. enteromorphae egg masses. 


C. D. Trowbridge, 1993 


Table 1 


Regression equations relating body length (mm) and wet 
weight (mg) of Aplysiopsis enteromorphae: log,)(weight) = 
m-log, (length) + 6, such that m and b are constants. The 
symbol n indicates the number of ascoglossans measured. 
The coefficient of determination, 7’, indicates the propor- 
tion of the variation accounted for by the regression line 
whereas the F and P values evaluate the statistical signif- 
icance of the line. 


Sites m b n r? F IP 


2.656 —2.265 16 0.885 107.9 <0.001 
1.945 —1.321 44 0.611 65.9 <0.001 
1.868 —0.913 60 0.434 44.5 <0.001 


Neptune Beach 
Strawberry Hill 
Two sites pooled 


proportion of ascoglossans <20 mg than did other samples: 
thus, recruitment appeared to be concentrated in June. 

Alderia modesta was a much smaller ascoglossan, ranging 
in size from 0.35 to 13.30 mg (wet weight) in the June 
1990 collection (Figure 3). Although skewed to the left, 
the size-frequency distribution appeared bimodal with small 
animals (1-2 mg) and larger conspecifics (4-6 mg) being 
the most common. On a local scale, however, A. modesta 
populations varied: size-frequency distributions of three 
randomly placed quadrats differed significantly (G-test, G 
= 42.0, 6 df, n = 148, P < 0.001). Although the sources 
of the ascoglossan size variation were not specifically ad- 
dressed, A. modesta tended to be much larger and more 
abundant on lush, dark green, velvety Vaucheria mats and 
smaller and less abundant on tough, hardened mats. Thus, 
herbivore size variation may reflect differences in quality 
of the local algal mat as food and substratum. Due to the 
substantial spatial variation, seasonal collections were not 
made: temporal variation in population structure would 
be obscured by high spatial variation. 


Length vs. Weight 


When two collections of Aplysiopsis enteromorphae from 
different sites were examined, the length-weight relation- 
ships differed (Figure 4A). At Neptune Beach, ascoglos- 
sans were much heavier for a given body length than 
conspecifics at Strawberry Hill (ANCOVA, F = 93.0, P 
< 0.001 on log-transformed data). When each site was 
considered separately, weight was directly related to body 
length (Table 1, P < 0.001). When data were pooled 
(Table 1), the relation was still significant although the 
association was more variable (7? = 0.434, P < 0.001). 
Based on size-frequency distributions and length-weight 
relations, the majority of individuals present during the 
summer were between 10 and 20 mm in length. 

For Alderia modesta (Figure 4B), wet weight was directly 
related to length (linear regression on log-transformed data, 
r? = 0.866, n = 148, F = 945.5, P < 0.001). Thus, modal 
sizes of A. modesta (Figure 3) corresponded to body lengths 
of 3-4 mm and 5-6 mm. Although the size data were based 


Page 103 


Alderia modesta 


No Egg Masses 
fa Egg Masses 


100 


80 


60 


40 


% of Ascoglossans 


20 


(Bes wy eee 


Wet Weight (mg) 
Figure 6 


Percentage of Alderia modesta producing egg masses in the lab- 
oratory (3 days, 11°C). Numbers above each bar denote number 
of individuals measured. 


on two collections (June and July 1990), the documented 
size range encompassed the observed range during other 
times of the year. Based on the asymptote for body length 
at ~6 mm (Figure 4B), maximum size of A. modesta in 
Yaquina Bay, Oregon was estimated as 6 mm. 


Reproduction 


The majority of Aplysiopsis enteromorphae produced egg 
masses in three days, irrespective of body size (Figure 5A). 
Even the smallest individual examined (4 mg wet weight) 
produced an egg mass in the laboratory. Furthermore, the 
weight of egg masses produced by each individual was 
clearly unrelated to ascoglossan size (Figure 5B, Spearman 
rank correlation, r, = 0.071, n = 72, P > 0.50). The lack 
of size-specific fecundity was not due to the imprecision 
of measuring wet weight: wet and dry weight values were 
highly correlated (Figure 5C, Pearson correlation, r = 
0.987, n = 72, P < 0.001). 

Alderia modesta also deposited egg masses in the labo- 
ratory. The proportion of individuals producing egg mass- 
es, however, was size specific (Figure 6). Most individuals 
<2 mg did not deposit eggs whereas almost all the ascoglos- 
sans >3 mg did. The minimum size of egg deposition was 
small: even the smallest A. modesta examined (0.45 mg) 
produced egg masses. 

The wet weight of Aplysiopsis enteromorphae egg masses 
was high, often exceeding that of the herbivore (Figure 
5B). This result suggests that the egg masses were hydro- 


Page 104 


philic, absorbing water upon deposition. In fact, about 94% 
of the egg mass wet weight was composed of water or other 
fluids (calculated from Figure 5C). In contrast, the egg 
masses of Alderia modesta appeared not very hydrophilic: 
most masses weighed <0.01 mg (level of detection), even 
for ascoglossans weighing several milligrams. 


DISCUSSION 
Life-History Attributes 


Opisthobranch life-history strategies have been cate- 
gorized as opportunistic (= exploitist) or equilibrium 
(MILLER, 1962; NYBAKKEN, 1974; CLARK, 1975). Many 
ascoglossan species belong to the former group (CLARK, 
1975). Specific opportunistic attributes include continuous 
recruitment, rapid growth, small size of reproduction, con- 
tinuous reproduction, and short life-span. The two species 
studied in Oregon apparently exhibit these traits. 

The rapid growth of Aplysiopsis enteromorphae can be 
estimated from the size-frequency distributions (Figure 2). 
If we make the simplistic assumption that modal size rep- 
resents ascoglossan growth in the preceding two weeks, 
then a rough estimate of the species’ growth rate would 
be ~10 mg/week or ~1.4 mg/day. This value is similar 
to the rate of 1.7 mg/day estimated for large (10 to 80 
mg) A. enteromorphae in the laboratory on Chaetomorpha 
(Trowbridge, unpublished data). Smaller animals presum- 
ably grow faster. 

These growth data suggest that Aplysiopsis enteromor- 
phae becomes sexually mature within a few days of meta- 
morphosis. Although the growth rate of Alderia modesta 
was not determined for Oregon populations, SEELEMANN 
(1967) reported that individuals from European popula- 
tions grew to sexual maturity (3 mm) in 10 days after 
metamorphosis. The minimum size of sexual maturity not- 
ed in this study (0.4 mg = 2 mm, Figure 4) was compa- 
rable. Early maturation has been reported for other as- 
coglossans as well. For example, Ercolania fuscata matured 
in <3 weeks at ~1 mg (CLARK, 1975), and Placida den- 
dritica matured at <1 mg (TROWBRIDGE, 1992b). Early, 
continuous egg production may ensure that most individ- 
uals produce offspring in spite of variable environmental 
conditions. 


Pool-Dwelling Ascoglossans 


Ascoglossan-algal associations exhibit striking parallels 
throughout temperate areas of the world. High intertidal 
pools with the green algae Cladophora and/or Chaetomor- 
pha are occupied by Aplysiopsis enteromorphae in the N.E. 
Pacific, Stiliger felinus (Hutton, 1882) in New Zealand, 
and Limapontia capitata (Miller, 1773) and L. senestra 
(Quatrefages, 1844) in the N.E. Atlantic (reviewed by 
TROWBRIDGE, in press). These species have a number of 
important similarities: they inhabit similar habitats, feed 


The Veliger, Vol. 36, No. 2 


on the same algal genera, and exhibit conspicuous rather 
than cryptic coloration. 

At first glance into a tidepool, Aplysiopsis enteromorphae 
may be mistaken for littorines and small mussels because 
of the black body with white highlights (Trowbridge, per- 
sonal observations). ROGINSKAJA (1984) made a similar 
observation, reporting that the black Limapontia capitata 
and L. senestra were conspicuous against the green algal 
hosts and looked superficially like young periwinkles and 
mussels. Finally, GARSTANG (1890) remarked that the black 
coloration of L. capitata “renders it at once noticeable” (p. 
422). The role of the black pigmentation is not clear. 
Perhaps it protects the ascoglossans from high light inten- 
sities, particularly ultraviolet radiation, in high intertidal 
habitats. Ascoglossan species with black pigmentation gen- 
erally have non-functional chloroplasts (CLARK et al., 1990), 
in contrast to the chloroplast symbiosis characteristic of 
many cryptic species. Because cladophoralean algae (Cla- 
dophora and Chaetomorpha) are structurally not suitable 
for chloroplast symbiosis (CLARK et al., 1990), the acqui- 
sition of black pigmentation in these high intertidal species 
was probably not constrained by chloroplast functionality. 

Two major differences, however, occur among these pool- 
dwelling species: body size and developmental mode. Aply- 
stopsis enteromorphae grows to 20 or 30 mm long (TROW- 
BRIDGE, in press). In contrast, Stiliger felinus grows to 10 
mm (POWELL, 1979), Limapontia capitata to 4 mm, and L. 
senestra to 8.5 mm (COLGAN, 1911; JENSEN, 1975; 
ROGINSKAJA, 1978). Thus, A. enteromorphae is consider- 
ably larger than its ecological counterparts. Furthermore, 
three of the species have planktotrophic larvae, whereas 
L. senestra has direct development (ROGINSKAJA, 1978; 
THOMPSON, 1976). Direct development would be advan- 
tageous for a high intertidal, pool-dwelling herbivore be- 
cause the species could form dense local populations on 
green algal hosts in individual pools or on emergent sub- 
strata. ROGINSKAJA (1978) suggested that this advantage 
of direct development may explain why the species is wide- 
ly distributed throughout the Barents and White seas. In 
contrast, planktotrophic larvae may have difficulty gaining 
access to the pools due to limited submergence time. For 
example, GARSTANG (1890) found L. capztata in pools that 
received fresh seawater (and, hence, larval ascoglossans) 
only during spring tides; the pools often dried up during 
neap tides. 


Algal-Mat Ascoglossans 


In high intertidal, estuarine environments, two ascoglos- 
sans are ecologically similar: Alderia modesta and Lima- 
pontia depressa Alder & Hancock, 1862. They inhabit 
Vaucheria mats (ENGEL et al., 1940; HARTOG, 1959; Va- 
DER, 1981), feed on the alga, are small, and are usually 
cryptically colored (but see HaRTOG [1959] for a review 
of color variation in L. depressa). Alderia modesta is <8 
mm in the N.E. Pacific (HAND & STEINBERG, 1955; Trow- 


C. D. Trowbridge, 1993 


bridge, this study) and <16 mm on North Atlantic shores 
(ENGEL et al., 1940; HARTOG, 1959; BLEAKNEY & BAILEY, 
1967; THOMPSON, 1976). Limapontia depressa is typically 
<6 mm long (THOMPSON, 1976). 

The egg mass sizes of Alderia modesta and Limapontia 
depressa overlap considerably (HARTOG, 1958) although 
the sizes of the adults producing the egg masses were not 
given. HAND & STEINBERG (1955) reported that egg masses 
of A. modesta were up to 5.5 mm long and the maximum 
size of the ascoglossans was 8 mm. Thus, the species de- 
posits egg masses of <69% of its body length. Furthermore, 
the fecundity of this species can be high: ~1000 eggs/day 
(SEELEMANN, 1967). 


Conclusions 


The N.E. Pacific Aplysiopsis enteromorphae is a large, 
black ascoglossan, often considerably larger than its eco- 
logical counterparts on other temperate shores. In contrast, 
Alderia modesta in Oregon is comparable in size to con- 
specifics from other geographic localities and to its coun- 
terpart, Limapontia depressa. On the basis of literature 
reports and the data presented herein, both species exhibit 
rapid growth rates and high fecundity. By comparing and 
contrasting species within each ascoglossan-algal assem- 
blage, insight will be gained as to the ecological and en- 
vironmental constraints affecting ascoglossan populations. 


ACKNOWLEDGMENTS 


I thank J. Lubchenco and L. Weber for providing facilities 
and support at the Hatfield Marine Science Center, Or- 
egon State University. Two anonymous reviewers made 
constructive comments on an earlier draft of this manu- 
script. The completion of this paper was supported by the 
Leigh Marine Laboratory, University of Auckland and a 
National Science Foundation grant INT-8888885ORO0 to 
the author. 


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CuiarK, K. B. 1975. Nudibranch life cycles in the Northwest 
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The Veliger 36(2):107-114 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Fine Structure of the Three Cell Types Found in the 
Digestive Gland of Elysia viridis 


(Opisthobranchia: Sacoglossa) 


REGINA GRIEBEL 


Institut fur Spezielle Zoologie und Vergleichende Embryologie der Universitat Munster, 
Hiufferstr. 1, D-4400 Minster, Germany 


Abstract. Three types of differentiated cells can be identified in the digestive gland (hepatopancreas, 
liver) of adult Elysia viridis (Montagu, 1804) with the aid of an electron microscope: digestive cells, 
microvilli cells, and cells with concentric-layered vacuole bodies. The last are called the “third cell type” 
in this study. The digestive cell, which has been the subject of many recent studies, contains chloroplasts 
derived from the food alga Codium fragile. The microvilli cell possesses a profuse and uniform brush 
border. The level pilose surface shows what appear to be pinocytotic invaginations, and apically the 
cytoplasm is interspersed with a large number of what are presumed to be pinocytotic vesicles. Large 
vacuoles containing osmiophilic granules occur in the basal half of the cell and sometimes seem to merge. 
The third cell type is described for the first time in a sacoglossan (although in pulmonate species the 
corresponding lime or calcium cell is common). Most of this cell is occupied by one or more vacuoles 
containing concentric layers of alternating electron-dense and electron-translucent material. These char- 
acteristic vacuoles are surrounded by copious rough endoplasmic reticulum. 


INTRODUCTION 


The digestive gland (hepatopancreas, liver) of Elysia viridis 
(Montagu, 1804) is a much-branched organ ramifying 
through every part of the body and ending blindly with 
innumerable small tubules directly under the epidermis. 
The relationship between the digestive gland and the green 
color of the slug was recognized early. SOULEYET (1852) 
noticed that the green substance found in the cells of the 
digestive gland of Elysia resembled the pigmentation of 
lower plants and DE NEGRI & DE NEGRI (1876) were 
able to substantiate this observation with experiments. KA- 
WAGUTI & YAMASU (1965) and TAYLOR (1968) were the 
first to show that the coloration of Elysza viridis is actually 
attributable to the ingested chloroplasts of the slug’s food, 
a siphonaceous alga. Since these studies, a large number 
of investigations have focused on various functional aspects 
such as the metabolic and photosynthetic processes of the 
digestive gland of Elysia. These have been summarized in 
HOFELMEIER (1985). 

Histological studies on the digestive gland of Elysza viri- 
dis began with HENNEGUY (1925). FRETTER (1940), in a 
study on the structure of the gut in three sacoglossans, 


confirmed HENNEGUY’s (1925) observations on Elysia and 
described extensively one cell type of the single-layered, 
endodermal epithelium, which she named “digestive cells.” 
It is the contents of these cells which give the slug its green 
color. A second cell type was briefly mentioned, but not 
clearly characterized. TAYLOR (1968), in a fundamental 
study of the ultrastructure and histochemistry of Elysia 
viridis, referred to FRETTER’s (1940) paper, confirmed the 
two cell types, and termed them “digestive cells” and “lime 
cells.” Recent reexamination of the fine structure of the 
digestive gland of Elysia viridis has revealed important 
disparities with the previously mentioned results and also 
with the results of the more recently published investi- 
gation by GRAVES et al. (1979) on the digestive gland of 
Elysia chlorotica. 

Few authors have worked on the fine structure of the 
digestive gland of the other opisthobranch orders: SCHME- 
KEL & WECHSLER (1968) showed four cell types (including 
an undifferentiated cell type) in the digestive gland of 
Trinchesia granosa. This means that I will be comparing 
my results chiefly with the findings of studies on the his- 
tology and ultrastructure of the digestive gland in proso- 


Page 108 


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The Veliger, Vol. 36, No. 2 


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Figure 1 


Diagram of the fine structure of the three cell types forming the epithelium of the digestive gland of Elysia viridis: 
the digestive cell (1), the microvilli cell (2), and the third cell type (3). 


branch and pulmonate gastropods, beginning with early 
authors, BARFUTH (1883), HIRSCH (1917), KRIJGSMAN 
(1928) and THIELE (1953), and dealing in particular with 
the more recent authors, ABOLINS-KRocIs (1961, 1965, 
1970), BANI (1962), SUMNER (1965, 1966a, b), WALKER 
(1970), and REYGROBELLET (1970). 


MATERIALS ann METHODS 


Specimens of Elysia viridis were collected on Codium fragile 
from the Mediterranean at Banyuls-sur-mer (France) and 
from the Atlantic coast at Roscoff (France). Before fixation, 
all 23 animals (length 2-15 mm) were anaesthetized for 
1 to 3 hr with 7% magnesium chloride in distilled water. 

The fixative used for routine light microscopy was 
Bouin’s fluid. After fixation, the material was dehydrated 
and embedded in paraffin. Sections were cut at 5, 6, or 7 
um and stained with either Heidenhain’s azan, Giemsa, 
Masson’s trichrome sequence, or Goldner’s triple se- 
quence. 

For electron microscopy, two fixation methods were used. 
Specimens were fixed either (1) in a solution of 0.5% 
potassium dichromate, 2% osmium tetroxide, and 70% 
double-filtered seawater, buffered to pH 7.2, or (2) 2.5% 
glutaraldehyde in Sgrensen’s phosphate buffer, followed 
by washing in Sgrensen’s phosphate buffer and postfixa- 


tion in 2% osmium tetroxide in 1.25% sodium hydrogen 
carbonate (CLONEY & FLOREY, 1968). 

After dehydration in graded series of acetone or ethanol 
with propylene oxide, specimens were embedded in Dur- 
cupan. Sections of 1 wm, cut on an LKB Ultrotome, were 
stained with 1% aqueous toluidine blue-1% aqueous borax 
solution at 80°C and used in the light microscope, often 
under phase-contrast for orientation. Sections of 600-900 
A, cut as noted before, were mounted on grids, stained 
with lead citrate following the procedure of REYNOLDS 
(1963), and then examined under a Philips EM 201 elec- 
tron microscope. Micrographs were taken at magnifica- 
tions from 500 to 24,000 times and enlarged photograph- 
ically to the required size. 


RESULTS 


The digestive gland of Elysza viridis consists of a single- 
layered epithelium bounded by a thin (0.5 um) basal lam- 
ina and supported by connective tissue and muscle fibres. 
The epithelium is composed of three different cell types: 
the digestive cell, the microvilli cell, and a third type of 
cell. The three types are readily told apart under the elec- 
tron microscope (Figure 4), by their position, their shape, 
the presence of microvilli or cilia, and by their cell content. 
All three cell types are found both in the main ducts of 
the digestive gland and in the epithelia of the small tubules 


Explanation of Figures 2 to 5 


Figure 2. Part of a transverse section through a digestive gland tubule composed of digestive cells (1), microvilli 
cells (2) with striking dense brush border, and the third cell type. Haemocoel (h); lumen of the digestive gland (1); 
concentric-layered vacuole body (vb). x 260 


Figure 3. Electron micrograph of portions of the brush border and the apical region of a microvilli cell and the 
cilia of the digestive cell, in longitudinal sections. Cilium (c); lumen (1); microvillus (mv); pinocytotic (?) invagination 
(pi); pinocytotic (?) vesicle (pv). x 13,000 


Figure 4. Electron micrograph of the three cell types of the epithelium of the digestive gland: digestive cell (1) with 
chloroplasts (cp), microvilli cell (2) with large vacuoles (va), and the third cell type (3). Basal lamina (b); concentric- 
layered vacuole body (vb); haemocoel (h); lumen (1). x 6800 


Figure 5. Electron micrograph of a microvilli cell; note the dense brush border and the content of the large vacuoles 
(va). Haemocoel (h); lumen (1). x 4500 


Page 110 


near the epidermis, but they do not display a uniform 
distribution. 


The Digestive Cell 


The digestive cell predominates in the epithelium of the 
digestive gland. It is easily recognized by the presence of 
chloroplasts, which are derived from the food of the slug 
and are found exclusively in this cell type. The digestive 
cell (Figures 1, 4) has a variable shape. Rectangular or 
triangular in outline, it averages about 9 wm in height and 
14 wm in width. The apex of the cell protrudes into the 
lumen of the tubule or is level with the apices of the 
epithelium, showing small, irregular indentations. 

The luminal border possesses an unkempt array of mi- 
crovilli (4-5 microvilli per wm of the plasmalemma) and 
bears long cilia (type 9+2). Usually only one cilium per 
digestive cell is present in section. Longitudinal or trans- 
verse sections of cilia are frequently observed in the lumen 
of the tubule (Figures 2, 3). The nucleus, which is oval 
or kidney shaped and sometimes deeply lobulated, mea- 
sures roughly 4.5 um in length and 2 wm in width. It lies 
much closer to the base than to the tip of the cell and has 
a distinct nucleolus. The double membrane, karyolymph, 
and chromatin are easy to recognize. The elongate mito- 
chondria (averaging 1 wm by 0.4 um) with cristae and the 
rough endoplasmic reticulum are common, the latter usu- 
ally near the base of the cell. Apically, the vacuolized 
cytoplasm contains many irregularly shaped vesicles; in 
the basal half of the cell, the cytoplasm is denser. 

Many digestive cells also contain some round or oval 
vacuoles of various sizes and appearances. There are small, 
electron-dense vacuoles (0.4 to 1.7 wm in diameter), larger, 
clearer vacuoles (1 to 3.5 wm in diameter) with homogenous 
contents or small osmiophilic granules, and irregularly 
shaped, electron-transparent vacuoles which appear “emp- 
ty.” These could also be extremely degenerated chloro- 
plasts. It is presumed that there are transitional forms. 

The round or oval-ellipsoid chloroplasts (Figure 4), 
measuring 1.5 to 4.5 um in length and 1.1 to 4.3 um in 
width, are bounded by a double membrane. Internally, 
they display a distinct lamellar structure. Apart from these 
lamellae, the clear homogenous matrix contains between 
one and eight small, round or oval granules, the so called 
plastoglobuli. Up to a third of the contents of a chloroplast 
may be taken up by the large, round or oval starch grains. 


The Microvilli Cell 


The microvilli cell (Figures 1, 2, 4, 5) is less common, 
usually rectangular in shape and averages about 11 um by 
9 um. It lies with a broad level surface next to the lumen 
of the tubule of the digestive gland. This border to the 
tubule lumen shows a characteristic profuse, well-defined 
and uniform array of microvilli (Figure 3). The length of 
the microvilli varies from 1.6 to 2.5 wm, but the microvilli 
of any one cell are always of equal length. The microvilli 
stand close together (8 or 9 microvilli per wm of the brush 
border) neither branching nor intermeshing. 


The Veliger, Vol. 36, No. 2 


Microvilli cells are devoid of cilia. The nucleus lies in 
the middle of the cell or towards the base. Mitochondria 
are present, and rough endoplasmic reticulum is usually 
distributed in the basal half of the cell. The microvilli cell 
typically has a dark “stained”? cytoplasm. This is inter- 
spersed with numerous small, round vesicles, presumably 
pinocytotic vesicles (Figure 3), below the luminal border 
in the apical region. The characteristic pinocytotic invag- 
inations are frequently observed. Lower down the cell, 
fewer and larger vesicles are scattered through the cyto- 
plasm. 

Two kinds of vacuoles are found in the microvilli cell 
(Figure 5): large, spherical or ellipsoid vacuoles, measuring 
2.8 to 6.5 wm in diameter or length, and small, round 
vacuoles, measuring 0.4 to 1.3 um in diameter. In sections, 
the bigger vacuoles usually occur in groups of three to five 
if medium-sized, or one to two if large-sized; the latter 
take up one-half to two-thirds of the cell volume. These 
vacuoles always have a distinct membrane, but diverse 
contents: a variable number of electron-opaque granules 
(averaging 1 um in diameter) may be scattered about the 
vacuole, which otherwise seems to be empty; other vacuoles 
display an accumulation of flaky, electron-dense material 
with no more than a few granules. The small vacuoles are 
densely packed with fairly uniform, electron-dense ma- 
terial containing a quantity of strongly osmiophilic gran- 
ules. Occasionally, larger vacuoles may be observed that 
contain globules the size of the small vacuoles described 
above. These globules vary a great deal in electron density, 
ranging from very compact to almost dispersed. Fusions 
of the large vacuoles may also occur. 


The Third Cell Type 


The third cell type (= “lime cell”), the rarest cell type 
in the epithelium of the digestive gland (Figures 1, 4, 6), 
occurs singly or in pairs. In sections, they are triangular 
or rectangular in shape and average 7 wm high and 11 wm 
wide. The base of the cell lies broadly on the basal lamina, 
and the tip, while directed towards the tubule lumen, does 
not always actually reach it. Cells of this third type seem 
to be displaced into the corners of the tubules of the di- 
gestive gland, occasionally protruding with a domed outline 
into the haemocoel. The apical surface of the cell, very 
rarely seen in sections, bears microvilli (Figure 6). 

The third cell type is characterized by the presence of 
large, clear vacuoles (Figures 7-9) occupying almost the 
entire cell volume. The vacuoles vary between 2 and 5 um 
in diameter. They are mostly spherical, sometimes ellip- 
soid, and are bounded by a unit membrane. The vacuoles 
contain a vacuole body (~ spherite of ABOLINS-KROGIS 
[1961, 1965, 1970], = spherule of SUMNER [1965, 1966a]) 
of electron-dense material with varied density and distri- 
bution which displays a conspicuous and characteristic 
concentric structure. The material lies directly beneath the 
unit membrane of the vacuole, or there may be a space 
between them. This can vary in extent from one vacuole 
to another but in any one vacuole the space around the 


R. Griebel, 1993 Page 111 


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at 


Explanation of Figures 6 to 9 


Figure 6. Electron micrograph of the third cell type reaching the lumen of the digestive gland (1) and containing 
three different concentric-layered vacuole bodies. x 7500 


Figure 7. Electron micrograph of a portion of the third cell type showing rough endoplasmic reticulum (r), which 
surrounds the vacuole with a concentric-layered vacuole body (vb); mitochondrion (m); vacuole or vesicle (v). 
x 16,000 


Figure 8. Electron micrograph of a vacuole with concentric-layered vacuole bodies; note the space between the 
vacuole membrane (vm) and the vacuole body (vb). x 37,000 


Figure 9. Electron micrograph of a vacuole with concentric-layered vacuole body showing regular rings of electron- 
dense material and a spherical center. Nucleus of the third cell type (n). x 28,000 


vacuole body is always constant. Further investigations on as uniform, more or less concentric rings (Figure 9). Or, 
live specimens will be necessary in order to establish whether within the membrane, there may be a number of diffuse 
this space is natural or artificial. rings lying close together, circumscribing a well-defined 

The material of the vacuole body may consist of alter- osmiophilic circle. In a third alternative, the material may 


nating electron-dense and translucent zones which appear consist of irregularly distributed flakes. 


Page 112 


The central part of the vacuole body appears either 
empty (Figure 8)—the contents possibly having been torn 
out during sectioning—or contains a compact, spherical 
core which may or may not have distinct edges (Figures 
6, 7, 9). In some vacuole bodies the rings, circles, and 
spherical cores may be excentrically shifted or less uni- 
formly structured than in the above description. Some vac- 
uole bodies even display two cores. In any one cell, the 
spherules can vary in size and appearance. Occasionally, 
I found vacuoles of normal size (2-5 wm) but lacking 
entirely a concentric-layered structure, and containing only 
a mixture of translucent, fine, and electron-dense flaky 
material. 

The vacuoles with concentric-layered vacuole bodies are 
always surrounded by rough endoplasmic reticulum (Fig- 
ure 7) which may be so abundant as to fill most of the 
cytoplasm. This cytoplasm is, in comparison with that of 
the digestive and microvilli cells, very clear and frequently 
uniform. The nucleus lies towards the base and presents 
a structure resembling that of the other two cell types. The 
shape of the nucleus seems to fit neatly into the space not 
occupied by the vacuoles. Thus, sometimes a sickle-shaped 
or club-shaped nucleus snuggles up closely to a vacuole. 
The extent of the Golgi apparatus of the third cell type is 
not yet known. 

Mitochondria are common in the third cell type. And 
there are also small “‘pigment(?)” vacuoles or vesicles av- 
eraging about 0.3 to 1 wm in diameter or length (Figure 
7). These are often round (rarely oval) in shape and contain 
either amorphous, completely electron-dense material or 
weakly osmiophilic material with granules in it enveloped 
in a distinct membrane. 


DISCUSSION 


The epithelium of the digestive gland of Elysia viridis is 
composed of cells of three distinct types—digestive cells, 
microvilli cells, and the third cell type, z.e., cells with con- 
centric-layered vacuole bodies. (A possible embryonic or 
undifferentiated cell is not considered in the present paper.) 
This calls into question the results of FRETTER (1940), 
TAYLOR (1968), and GRAVES e¢ al. (1979), all of whom 
found only two cell types in the digestive gland of Elysza. 

One hypothesis is that we are confronted here not with 
different cell types, but with different phases of the cell 
cycle of a single cell type, as reported by GRAHAM (1938) 
for the three aeolids Eolidina alderi, Facelina drummondi 
and Cratena glotensis, by SUMNER (1965, 1966a, b) for 
Helix aspersa, Succinea putris, Testacella mangei and Ano- 
donta anatina, and by REYGROBELLET (1970) for Limax 
maximus. My investigations on Elysia do not support this 
phase theory. 

Digestive cells, which are the most plentiful type, ac- 
cumulate chloroplasts derived from the food of Elysia, the 
green alga Codium fragile. Here, they are in part digested 
and in part used in photosynthesis. Since the digestive cell 
and particularly their chloroplasts have been the object of 


The Veliger, Vol. 36, No. 2 


many studies over the last twenty years, a more detailed 
discussion of the function of this cell type would be su- 
perfluous. 

Homologies of the digestive cell are not difficult to find: 
“Leberzelle” of BARFUTH (1883), “digestive cell” of FRET- 
TER (1940) and TayLor (1968), and ““B-Zelle (Verdau- 
ungszelle)” of SCHMEKEL & WECHSLER (1968). The di- 
gestive cell bears apically a small number of large cilia, as 
observed by HENNEGUY (1925), and several microvilli. The 
nucleus lies towards the base and has a distinct nucleolus. 
These observations have already been reported by FR- 
ETTER (1940) and TAYLOR (1968). 

FRETTER (1940), examining live specimens, also re- 
ported observing brown or yellowish granular clumps con- 
tained in vacuoles below the distal ends of most digestive 
cells. She regarded them as excretory masses, which are 
released from the cells and then passed through the ducts 
of the digestive gland to the intestine and thence to the 
anus, where they are expelled. TAYLOR (1968) also noticed 
these brown or yellowish vacuoles in living cells and, under 
the light microscope, described them as being filled with 
an amorphous substance. In electron microscopy he found, 
close to the basal lamina, large, clear, apparently com- 
pletely empty vacuoles surrounded by complexes of rough 
endoplasmic reticulum. He suggested that the emptiness 
could be the result of extraction during the preparation of 
the slugs. I found no such “empty” vacuoles in the digestive 
gland of Elysza. Obviously, FRETTER’s (1940) cell with 
brown or yellowish vacuoles is analogous to my second cell 
type, the microvilli cell, and TayLor’s (1968) vacuoles 
with the enormous complex of endoplasmic reticulum, ob- 
served under the electron microscope, to my third cell type. 

The microvilli cell possesses a strikingly dense and uni- 
form array of microvilli. Below the luminal border many 
presumably pinocytotic vesicles occur abundantly dis- 
persed throughout the apical half of the cell. Deeper in 
the cell there are much larger vacuoles which may merge 
and often contain large, osmiophilic granules. 

FRETTER’s (1940) second cell type, which she describes 
briefly and generally, may be either my second cell type 
(the microvilli cell), or my third cell type with the con- 
centric-layered vacuole bodies. TAYLOR’s (1968) descrip- 
tion of his second cell type, together with his measurements 
of it, coincide with my observations of my second cell type. 
However, he calls these cells ‘“‘lime cells,” a term I would 
rather reserve, following the literature cited below, for the 
designation of my third cell type. 

Looking beyond Elysia, numerous other homologies ex- 
ist within the opisthobranchs. Based on light microscopy, 
there are, for example, “‘cellules vacuolaires excrétices” of 
HECHT (1895), ‘“‘cellules vacuolaires” of ROUSSEAU (1935), 
and the “cells with excretion as main function” of 
BURGIN-Wyss (1961). SCHMEKEL & WECHSLER (1968), 
in one of the first studies of the digestive gland of an 
opisthobranch, Trinchesia granosa, based on electron mi- 
croscopy, described the ‘““D-Zelle” as possessing a profuse 
brush border and vacuoles with osmiophilic granules. 


R. Griebel, 1993 


Page 113 


Schmekel & Wechsler considered excretion to be the main 
function of this cell type. 

The literature of pulmonates, and indeed of all gastro- 
pods, provides many descriptions of cells similar to the 
microvilli cell. These can, however, be only briefly men- 
tioned here. The first worker on the digestive gland of 
pulmonates, BARFUTH (1883), suggested that the ‘“‘Fer- 
mentzelle” of Arion and Helix secretes enzymes. Later 
authors, for example THIELE (1953, on many pulmonates, 
several prosobranchs, and two opisthobranchs) and SUMNER 
(1965, on Helix aspersa) believed it to be excretory. WALK- 
ER (1970) came to similar conclusions in studying the 
digestive gland of Agriolimax reticulatus. His “excretory 
cell” closely corresponds in appearance to the microvilli 
cell of Elysia. I suggest that this cell takes up substances 
from the tubule lumen by pinocytosis and seals them in 
the vesicles, and that these vesicles then merge to form 
larger vacuoles until one large “‘telosomal” vacuole fills up 
nearly the entire cell. The presence of a profuse and dense 
brush border supports the hypothesis of a resorptive func- 
tion in the microvilli cell. That the microvilli cell of Elysia 
releases the large vacuole into the lumen of the digestive 
gland for final excretion out of the body of the slug can as 
yet only be assumed. In 77inchesia granosa an exocytosis 
of the dark telosomal, “pigment” granules never takes 
place. Instead, they are accumulated until death (SCHME- 
KEL & WECHSLER, 1968). 

The third cell type has not previously been described in 
Elysia viridis. Furthermore, only two cell types have been 
reported to date within the sacoglossans. In this respect, 
the sacoglossans differed from most of the other gastropods. 
My investigations show that a third cell type is present. 

Cells of the third type lie displaced towards the base of 
the epithelium, rarely reaching the tubule lumen. In sec- 
tions, they are triangular or rectangular in shape and are 
further characterized by the presence of round or oval 
vacuoles with typical concentric-structured contents. These 
vacuoles are surrounded by copious rough endoplasmic 
reticulum, which occasionally fills nearly the entire cell. 

The “C-Zelle” of the aeolid Trinchesia granosa (SCHME- 
KEL & WECHSLER, 1968) corresponds nearly completely 
to the third cell type of Elysza in position, shape, extent of 
endoplasmic reticulum and finally in the presence of large 
vacuoles with diffuse, concentrically arranged, weakly os- 
miophilic content. The lime cells of the pulmonates show 
similar characteristics; ABOLINS-KRoGIs (1961, 1965, 1970) 
on Helix, REYGROBELLET (1970) on Limax, and WALKER 
(1970) on Agriolimax reported cells with vacuoles contain- 
ing concentric layers of alternating electron-dense and elec- 
tron-translucent material. The illustrations in these studies 
look identical to those of Elysza. Therefore, the name “lime 
cell” should be reserved for this cell type, rather than as 
in TAYLOR (1968). 

While ABOLINS-KRoGIs (1961, 1965, 1970), as also BANI 
(1962) on Vaginulus borellianus, observed the central area 
to be filled-with electron-dense material, WALKER (1970) 
could not establish this in Agriolimax. In the sections of 


Elysia I frequently found spherical cores. ABOLINS-KROGIS 
(1965) believed that the “emptiness” of a vacuole could be 
a result of fixation and referred to the methods of 
BOOTHROYD (1964) for prevention of the decalcification 
of the vacuoles. ABOLINS-KRocIs (1961, 1965) described 
the “calcium spherites” of the “calcium cell” in Helix as 
consisting of an organic matrix in which inorganic salts 
are deposited. Later (1970), she described the origin and 
formation of the “calcium spherites.” She regarded the 
different-looking but always concentrically structured vac- 
uole bodies as different developmental stages. In my opin- 
ion, this also applies to the vacuole bodies of Elysza. 

The function of the third cell type in most gastropods 
and in Elysia is still undetermined. In the early days, 
BARFUTH (1883) believed that the calcium was utilized in 
shell repair in Helix, and later workers, for example 
ABOLINS-KRoGIs (1961, 1965), also put forward this the- 
ory. This function must be ruled out for the shell-less 
sacoglossan Elysia, and in most of my specimens cells of 
the third type were too well developed to be a relict of 
phylogenesis. 

HIRSCH (1917) suggested that the spherules acted as a 
buffer reserve regulating the pH of the digestive tract in 
Murex, Natica, Pterotrachea, and Pleurobranchea, and 
KRIJGSMAN (1928) shared this view for Helix. SCHMEKEL 
& WECHSLER (1968, on Trinchesia granosa) assumed se- 
cretion to be the general function of the vacuoles, which I 
accept for Elysia. Furthermore, I consider WALKER’s (1970) 
proposition very interesting. He suggests that the lime cells 
act as a store of calcium which is utilized in mucus pro- 
duction as well as for the metabolism of the body in general. 
He referred to investigations proving that the mucus con- 
tains granules of calcium, which it is claimed make the 
mucus more viscous. This might well be one of its functions 
in Elysia: the tubules of the digestive gland occasionally 
seem to lie close to the mucous cells of the epidermis. 
Sometimes even the basal lamina of the ectoderm and of 
the endoderm seem contiguous and the haemolymph space 
becomes exceedingly narrow. 

Further studies on this third type of cell will be necessary 
to determine its proper function. It may be, perhaps, that 
for each group it performs a different function. 


ACKNOWLEDGMENTS 


I wish to express my gratitude to Prof. Dr. Luise Schme- 
kel for support and guidance and for her critical review 
of the manuscript. The hospitality of the Laboratoire Ara- 
go, Banyuls-sur-mer (France), and the Station biologique, 
Roscoff (France), is gratefully acknowledged. I also thank 
Gerhard Nagel for operating the electron microscope and 
Ken Wilson for reviewing this paper. 


LITERATURE CITED 


ABOLINS-Krocis, A. 1961. The histochemistry of the hepato- 
pancreas of Helix pomatia (L.) in relation to the regeneration 
of the shell. Arkiv for Zoologi 13:159-202. 


Page 114 


ABOLINS-Krocis, A. 1965. Electron microscope observations 
on calcium cells in the hepatopancreas of the snail, Helix 
pomatia, L. Arkiv for Zoologi 18:85-92. 

ABOLINS-KRrocIs, A. 1970. Electron microscope studies of the 
intracellular origin and formation of calcifying granules and 
calcium spherites in the hepatopancreas of the snail, Helix 
pomatia L. Zeitschrift fur Zellforschung 108:501-515. 

BaNI, G. 1962. Struttura e ultrastruttura dell’epatopancreas di 
Vaginulus borellianus (Colosi). Monitore zoologico Italiano 
69:157-171. 

BaRrFUTH, D. 1883. Uber den Bau und die Tatigkeit der Gas- 
tropodenleber. Archiv fur mikroskopische Anatomie 22:473- 
524. 

BooTHROYD, B. 1964. The problem of demineralisation in thin 
sections of fully calcified bone. Journal of Cell Biology 20: 
165-173. 

Burcin-Wyss, U. 1961. Die Ruckenanhange von 77rinchesia 
coerulea (Montagu). Revue Suisse de Zoologie 68:461-582. 

Coney, R. A. & E. FLorey. 1968. Ultrastructure of cepha- 
lopod chromatophore organs. Zeitschrift fur Zellforschung 
89:250-280. 

De NeEcrI, A. & G. DE NEGRI. 1876. Farbstoffe aus Elysia 
viridis. Berichte der deutschen chemischen Gesellschaft 9(1): 
84-85. 

FRETTER, V. 1940. On the structure of the gut of the ascoglossan 
nudibranchs. Proceedings of the Zoological Society of Lon- 
don 110:185-198. 

GRAHAM, A. 1938. The structure and function of the alimentary 
canal of aeolid molluscs with a discussion on their nema- 
tocysts. Transactions of the Royal Society of Edinburgh 59: 
267-307. 

Graves, D. A., M. A. GIBSON & J. S. BLEAKNEY. 1979. The 
digestive diverticula of Alderia modesta and Elysia chlorotica 
(Opisthobranchia: Sacoglossa). The Veliger 21:415-422. 

HecutT, E. 1895. Contribution a l’étude des nudibranches. 
Mémoires de la Société zoologique de France 8:539-711. 

HENNEGUY, L. F. 1925. Contribution a Vhistologie des nudi- 
branches. Archives d’Anatomie microscopique et de Mor- 
phologie expérimentale 21:400-466. 

Hirscn, G. C. 1917. Die Ernahrungsbiologie fleischfressender 
Gastropoden. I. Makroskopischer Bau, Nahrung, Nah- 
rungsaufnahme, Verdauung, Sekretion. Zoologische Jahr- 
biicher, Abteilung Allgemeine Zoologie und Physiologie 35: 
357-504. 

HOFELMEIER, R. 1985. Bau der Mitteldarmdruse von Elysia 


The Veliger, Vol. 36, No. 2 


viridis (Sacoglossa, Opisthobranchia). Master’s Thesis, Uni- 
versity of Munster. 83 pp. 

KawacGutTI, S. & T. YaMasu. 1965. Electron microscopy on 
the symbiosis between an elysioid gastropod and the chlo- 
roplasts of a green alga. Biological Journal of Okayama 
University 11:57-65. 

KRIJGSMAN, B. J. 1928. Arbeitsrhythmus der Verdauungsdri- 
sen bei Helix pomatia. II. Sekretion, Resorption und Phag- 
ocytose. Zeitschrift fiir vergleichende Physiologie 8:187-280. 

REYGROBELLET, D. 1970. Les effets du jeune sur |’hépatopan- 
creas de Limax maximus L. Bulletin de la Société Zoologique 
de France 95(2):329-333. 

REYNOLDS, E. S. 1963. The use of lead citrate at high pH as 
an electronopaque stain in electron microscopy. Journal of 
Cell Biology 17:208-212. 

ROUSSEAU, CH. 1935. Histophysiologie du foie des Eolidiens. 
Archives d’Anatomie microscopique et de Morphologie ex- 
perimentale 31:304-395. 

SCHMEKEL, L. & W. WECHSLER. 1968. Feinstruktur der Mit- 
teldarmdrtise (Leber) von Trinchesia granosa (Gastropoda 
Opisthobranchia). Zeitschrift ftir Zellforschung 84:238-268. 

SOULEYET, F. L. A. 1852. Voyage autour du monde exécuté 
pendant les années 1836 et 1837 sur la corvette La Bonité. 
In: F. Eydoux, Zoologie par Eydoux et Souleyet, Vol. 2. 
Bertrand: Paris. 

SUMNER, A. T. 1965. The cytology and histochemistry of the 
digestive gland cells of Helix. Quarterly Journal of Micro- 
scopical Science 106(2):173-192. 

SUMNER, A. T. 1966a. The fine structure of digestive gland 
cells of Helix, Succinea and Testacella. Journal of the Royal 
Microscopical Society 85:181-192. 

SUMNER, A. T. 1966b. The fine structure of the digestive gland 
cells of Anodonta. Journal of the Royal Microscopical Society 
85:417-423. 

TayLor, D. L. 1968. Chloroplasts as symbiotic organelles in 
the digestive gland of Elysia viridis (Gastropoda Opistho- 
branchia). Journal of the Marine Biological Association of 
the United Kingdom 48:1-15. 

THIELE, G. 1953. Vergleichende Untersuchungen tber den 
Feinbau und die Funktion der Mitteldarmdrtise einheim- 
ischer Gastropoden. Zeitschrift fir Zellforschung 38:87-138. 

WALKER, G. 1970. The cytology, histochemistry, and ultra- 
structure of the cell types found in the digestive gland of the 
slug, Agriolimax reticulatus (Miller). Protoplasma 71:91- 
109. 


The Veliger 36(2):115-123 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Behavioral Interactions Among Nudibranchs Inhabiting 


Colonies of the Hydroid Obelia geniculata 


by 


WALTER J. LAMBERT' 


Department of Zoology, University of New Hampshire, Durham, New Hampshire 03824, USA 


Abstract. 


Behavioral interactions among four species of nudibranchs (Dendronotus frondosus, Doto 


coronata, Eubranchus exiguus, and Tergipes tergipes) were studied to determine whether interference 
governs their distributions and feeding locations within colonies of the hydroid Obelia geniculata. Initial 
behaviors displayed by nudibranchs when approaching other nudibranchs were similar. Nudibranchs 
initiated contact by touching with the rhinophores or apparent “tasting” with the oral lobes. Encounters 
were brief, and the response of any nudibranch to contact varied, but was generally non-aggressive. 
Nudibranchs were not displaced from an area within a hydroid colony by heterospecific nudibranchs. 
The locations of Tergipes, Dendronotus, and Doto were affected by an increased density of conspecifics, 
but this pattern was inconsistent. Interspecific interactions between nudibranchs did not dictate where 
a nudibranch fed within the hydroid colony. In particular, the apparent lack of a limiting resource and 
the absence of aggressive interactions among individuals suggest that competition is unimportant in this 


community. 


INTRODUCTION 


Spatial dispersion and aggression have a great impact on 
the abundance and population dynamics of animals (BROWN 
& ORIANS, 1970; KING, 1973). Aggressive behavioral en- 
counters among species in a community often determine 
the use of resources by those species. For example, in 
terrestrial communities aggression by stem boring insects 
(RATHCKE, 1976), dung beetles (BARTHOLOMEW & HEIN- 
RICH, 1978), and slugs (ROLLO & WELLINGTON, 1979) 
limits access to food resources and shelters of congeners 
and others. In those studies when individuals of different 
species interact, attacks by the superior individual resulted 
in injury or death of the subordinate. In other studies, 
interactions among species may be infrequent and occur 
only at high population densities. Experimental increases 
in densities of land snails depress activity and survival both 
of conspecifics and heterospecifics by interfering with feed- 
ing (SMALLRIDGE & Kirsy, 1988; BAUR & Baur, 1990). 
Each of these cases describes interference competition, where 
the actions of individuals directly affect how other species 
use resources. 


' Present address: School of Biological & Medical Sciences, 
Gatty Marine Lab, University of St. Andrews, St. Andrews KY16 
8LB, Scotland. 


In marine intertidal habitats, aggressive encounters be- 
tween gastropods restrict movements to particular areas of 
the shore. The Pacific mud snail Cerithidea californica 
(Haldeman) is confined to marsh pans in San Francisco 
Bay by behavioral avoidance of Ilynassa obsoleta (Say) 
(RACE, 1982). In Barnstable Harbor, Massachusetts, the 
periwinkle Littorina littorea (L.) limits the microhabitat 
distribution of J. obsoleta in the mid-intertidal zone 
(BRENCHLEY & CARLTON, 1983). Littorina littorea arouses 
I. obsoleta by grazing on its shell epiflora and this behavior 
interferes with the foraging, locomotory, and reproductive 
activities of the native snail. Aggressive interactions be- 
tween limpets (Patella spp.) prevent access for home scars 
and territories on rocks (BRANCH, 1975, 1981). Although 
behavioral interactions among gastropods affect distribu- 
tions in some systems, the phenomenon is not universal 
(WALDEN, 1981; CHOAT & ANDREW, 1986; BERMAN & 
CARLTON, 1991). 

In marine epifaunal communities, hydroids provide food 
and habitat for many small, motile invertebrates, especially 
nudibranch mollusks (CLARK, 1975; LAMBERT, 1985). Nu- 
dibranchs either graze and crop polyps or penetrate the 
outer skeleton and suctorially remove the soft tissue 
(NYBAKKEN & MCDONALD, 1981; LAMBERT, 1991a). The 
majority of nudibranchs within hydroid colonies are small 
(<5 mm), cryptic species. The abundance and presence of 


Page 116 


HB Reactions to Heterospecifics (n=73) 


L] Reactions to Conspecifics (n=11) 


T-NR T-Cl T-Av T-Cr Ta-Cl Ta- Av Ta-NR Bri-NR Avoid 


HB Responses of Heterospecifics (n=58) 
LC Responses of Conspecifics (n=11) 


80 


60 


% Total Interactions 
ow 


40 
20 
0 
T-NR T-Av T-Bn T-T Ta-NR Ta-Av_ Bn-Av 
Behaviors 
Figure 1 


A. Behaviors of Dendronotus frondosus before and after initiating 
an encounter with other nudibranchs on colonies of Obelia gen- 
iculata. B. The responses of other nudibranchs to interactions 
with D. frondosus. (T = touch, Ta = taste, Cl = climb, Bri = 
bristle cerata, Cr = cringe, Av = avoid/aversion, NR = no re- 
action) 


particular species of nudibranchs are often unpredictable, 
but when multiple species are present competition for food 
and habitat space seems likely. 

In the southern Gulf of Maine, blades and stipes of the 
kelps Laminaria saccharina (L.) Lamour. and L. digitata 
(Huds.) Lamour. are often covered by the campanularid 
hydroid Obelia geniculata (L.). At least four species of 
nudibranchs are frequent predators and inhabitants of col- 
onies of Obelia spp. in northern New England: Dendronotus 
frondosus (Ascanius, 1774), Doto coronata (Gmelin, 1791), 
Eubranchus exiguus (Alder & Hancock, 1848), and Ter- 
gipes tergipes (Forskal, 1775) (SWENNEN, 1961; CLARK, 
1975; Topp, 1981; LAMBERT, 1991b). Encounters among 
these nudibranchs occur frequently, but the extent to which 
such interactions dictate how each species uses the hydroid 
colony is unknown. The present study assesses the behav- 
ioral interactions among the nudibranchs. The potential 
for interference to determine nudibranch distributions and 
feeding locations within the hydroid colony is discussed 
with respect to possible mechanisms of the species’ coex- 
istence in the community. 


The Veliger, Vol. 36, No. 2 


Joke 
BB Reactions to Heterospecifics (n=48) 
(J Reactions to Conspecitics (n=9) 

N 

=) 

o 
om 

— 

1S) 

foe) 

bal 

oO 

— 

a) T-NR T-Cl T-Av T-T  Ta-NR Ta-Av Avoid 
— B 4 

fos} 

— 100 a 

jo) HB Responses of Heterospecitics (n=42) 
Ea L] Responses of Conspecifics (n=6) 
we 8 


60 
40 
20 
0 
T-NR T-Ta T- Av T-Cr Ta-NR Ta-Av 
Behaviors 
Figure 2 


A. Behaviors of Doto coronata before and after initiating an en- 
counter with other nudibranchs on colonies of Obelia geniculata. 
B. The responses of other nudibranchs to interactions with D. 
coronata. (T ='touch, Ta = taste, Cl = climb, Cr = cringe, Av 
= avoid/aversion, NR = no reaction) 


MATERIALS ann METHODS 


Nudibranchs and hydroids were collected from a shallow 
(4-10 m), subtidal kelp bed at Cape Neddick, York, Maine, 
USA (43°10'N, 70°36'W) during May-September, 1989 
(water temperatures: 10-18°C). Kelp blades were removed 
from stipes and placed in plastic bags while underwater. 
In the laboratory, nudibranchs were isolated by species 
and kept in mesh containers in flowing seawater tanks. 
Hydroid colonies were also kept in flowing seawater tanks 
until needed. 


Behavioral Interactions 


Nudibranchs were placed on portions of kelp blades 
covered with Obelia geniculata in 10-cm-diameter stacking 
dishes. Interactions between nudibranchs were observed 
with a stereo microscope and recorded. Behaviors were 
categorized into the following patterns (after ALLMON & 
SEBENS, 1988): (1) touch (contact of oral tentacles or rhino- 
phores with the other nudibranch), (2) “taste” (contact of 
mouth with another nudibranch), (3) climb (movement of 
a nudibranch over or onto the back of another nudibranch), 


W. J. Lambert, 1993 


Page 117 


(4) cringe (quick, muscular contraction of a nudibranch’s 
body), (5) aversion or avoidance (movement away from 
another nudibranch), (6) bristle (the erection or movement 
of cerata toward another nudibranch), and (7) no reaction 
(NR) (either only the temporary retraction of rhinophores 
or no apparent movement). 


Displacement and Nearest Neighbor 


Pair-wise manipulative experiments tested whether the 
location of a nudibranch within a colony differed when 
among conspecifics or heterospecifics. Nudibranch densi- 
ties in each treatment were consistent with field densities. 
The densities used for each species pair were, for Tergipes : 
Dendronotus (7:1), Tergipes : Doto (8:1), Dendronotus : Doto 
(6:1), and Doto : Eubranchus (2:3). Two combinations of 
species—Tergipes : Eubranchus (8:1) and Dendronotus : 
Eubranchus (5:1)—were not tested due to their unavail- 
ability. 

Interspecific treatments were performed by separately 
placing nudibranchs of two species (A, B) onto three mi- 
croscope slides with pieces of Obelia-covered kelp attached. 
Species A was introduced to the slides and allowed 24 hr 
to become established. Slides were suspended in open slide 
trays in an aquarium at ambient seawater temperature. 
After 24 hr the location of each nudibranch was docu- 
mented. Four parameters identified the location of each 
nudibranch: height on an upright, density of hydrocauli 
in a 1 cm? area around the nudibranch, the distance be- 
tween any two nearest nudibranchs (nearest neighbor), 
and the identity of the nearest neighbor. Hydrocaulus den- 
sity was quantified to characterize the horizontal area of 
the colony occupied by a nudibranch. After the locations 
of individuals of species A were recorded, species B was 
introduced to the hydroid colony and the slides were re- 
suspended in aquaria for 24 hr. The removal and replace- 
ment of slides did not appear to disturb the nudibranchs; 
they were not dislodged from the hydroid colony. The 
location of each nudibranch was then again documented. 
A reciprocal pair-wise treatment was run simultaneously, 
allowing species B to establish first. To control for intra- 
specific interactions, monospecific treatments were con- 
ducted. Protocols were identical to heterospecific treat- 
ments and were run simultaneously. 

Analysis of variance was utilized in a randomized block 
design (ZAR, 1984) to determine whether the location of 
a nudibranch differed when among conspecifics and het- 
erospecifics. The pattern of spatial dispersion of individ- 
uals of each species of nudibranch was determined at both 
field densities and following an increase above field den- 
sities using nearest neighbor methods (CLARK & EVANS, 
1954). 


RESULTS 
Behavioral Interactions 


When approaching another nudibranch, the initial be- 
haviors displayed by individuals of each species were sim- 


BB Reactions to Heterospecifics (n=33) 
LJ Reactions to Conspecifics (n=3) 


T-NR T-T T-Av T-Cr Ta-NR_ Ta-Cl = Avoid 


Wi Responses of Heterospecifics (n=32) 
CL Responses of Conspecifics (n=3) 


% Total Interactions 


T-NR T-T T-Av T-Cr 
Behaviors 
Figure 3 


A. Behaviors of Eubranchus exiguus before and after initiating an 
encounter with other nudibranchs on colonies of Obelia geniculata. 
B. The responses of other nudibranchs to interactions with E. 
exiguus. (T = touch, Ta = taste, Cl = climb, Cr = cringe, Av = 
avoid/aversion, NR = no reaction) 


ilar (Figures 1-4). Encounters usually occurred while one 
nudibranch was crawling across the kelp surface, whereas 
meetings between any two nudibranchs on a hydrocaulus 
were infrequent. On almost all occasions contact between 
heterospecifics involved the rhinophores or oral tentacles 
(Touch) or the mouth (Taste). These behaviors were non- 
aggressive and seemingly exploratory. Encounters were 
brief and the response of any nudibranch to contact varied, 
but both the initiator and the recipient generally reacted 
non-aggressively (62.1% and 81.4%, respectively). Actual 
aggressive behaviors and responses (bristling cerata or 
cringing) were infrequent and movements of an avoiding 
nudibranch were not different from the actions of a nu- 
dibranch climbing over another. The individual behavioral 
patterns for each species of nudibranch are described be- 
low. 


Dendronotus frondosus 


Dendronotus frondosus crawled across the kelp surface 
and among hydrocauli almost continuously; individuals 
were sedentary only when feeding. When D. frondosus 
approached another nudibranch any encounter was ini- 


Page 118 


The Veliger, Vol. 36, No. 2 


A. 
50 
BB Reactions of Heterospecifics (n=77) 
40 LC) Reactions of Conspecifics (n=7) 
30 
20 
10 
B T-NR T-Bn T-Cl T-Av T-Ta Ta-NR Ta-Av Bri-NR Avoid 


fe) 
o 


60 


% Total Interactions 


40 


20 


T-Nr T- Av T-Cr T-Ta Ta-NR Bn-Cr 
Behaviors 
Figure 4 


A. Behaviors of Tergipes tergipes before and after initiating an 
encounter with other nudibranchs on colonies of Obelia geniculata. 
B. The responses of other nudibranchs to interactions with 7. 
tergipes. (T = touch, Ta = taste, Cl = climb, Bri = bristle cerata, 
Cr = cringe, Av = avoid/aversion, NR = no reaction) 


tiated by contact with the oral tentacles or rhinophores, 
regardless of species (Figure 1). Following contact with 
another nudibranch, D. frondosus usually retracted its rhi- 
nophores, resulting in a “‘no reaction” response, or climbed 
over the other nudibranch (z.e., continued moving in the 
same direction) (Figure 1A). These responses to initial 
contact were, however, inconsistent. In 25% of the en- 
counters with heterospecifics, D. frondosus turned away 
(Aversion) after initiating an encounter, and in 19% of the 
encounters D. frondosus turned away before any contact 
was made. These latter interactions occurred when D. 
frondosus was within close proximity (2-3 mm) of the other 
nudibranch. 

The responses of nudibranchs to advances by Dendrono- 
tus frondosus were usually non-aggressive (Figure 1B). Most 
reactions involved simply a retraction of the oral tentacles 
or rhinophores by all species (NR). Heterospecifics were 
seldom displaced by D. frondosus, but conspecifics turned 
away in 46% of encounters. 


Doto coronata 


Individuals of Doto coronata were sedentary. It was com- 
mon for any individual to remain atop a stolon for 2-3 hr 
during any observational period. Encounters initiated by 


D. coronata were very similar and D. coronata touched the 
other nudibranch in 82.5% of encounters (Figure 2). Most 
often (67%) D. coronata followed contact behavior by re- 
tracting its rhinophores (NR) or by climbing (11%) over 
the other nudibranch (Figure 2A). Doto coronata occasion- 
ally retreated from encounters. Aversion behavior, as pre- 
viously described for Dendronotus frondosus, occurred in 
13% of encounters. 

Reactions of heterospecifics to an encounter initiated by 
Doto coronata were variable (Figure 2B). Although nudi- 
branchs most frequently did not react (64%), they did turn 
away in approximately 25% of interactions with D. coro- 
nata. The immediate behavior of conspecifics to D. coronata 
was one of no reaction (Figure 2B), and often the two 
nudibranchs then proceeded to copulate. 


Eubranchus exiguus 


When Eubranchus exiguus approached another nudi- 
branch it initiated contact by touching (77%) or tasting 
(11%) and subsequently did not respond in 70% of these 
encounters (Figure 3A). Eubranchus exiguus avoided con- 
tact in 15% of all possible encounters. Reactions of E. 
exiguus to conspecifics were similar to the above pattern, 
and were not aggressive (Figure 3A). 

Heterospecific nudibranchs did not respond to advances 
by Eubranchus exiguus in 91% of all encounters (Figure 
3B). These nudibranchs appeared undisturbed and at most 
only retracted their rhinophores. Reactions of conspecifics 
to E. exiguus were non-aggressive; nudibranchs either did 
not respond (66%) or touched E. exiguus with the oral 
tentacles (33%) (Figure 3B). 


Tergipes tergipes 


Individuals of Tergipes tergipes were active; they crawled 
continuously across the kelp surface and up and down 
hydrocauli, stopping only briefly to feed on an exposed 
polyp. Most encounters initiated by 7. tergipes were by 
either touching another nudibranch with the oral tentacles 
and rhinophores (68%) or tasting (11%) (Figure 4A). An 
aggressive behavior (bristling cerata at a heterospecific) 
was elicited very infrequently (3%). In cases where a re- 
sponse was elicited, 7. tergipes reacted to encounters with 
other nudibranchs by retracting its rhinophores (NR) 
(45%). Tergipes tergipes turned away before meeting an- 
other nudibranch in 21% of cases and turned away after 
it initiated an interaction in 26% of encounters. Intraspe- 
cific encounters resulted in non-aggressive reactions by 7. 
tergipes in all interactions (Figure 4A). 

The majority of reactions of heterospecifics to Tergipes 
tergipes was retraction of rhinophores (NR) (84%) (Figure 
4B). Conspecifics never reacted aggressively to an approach 
by another nudibranch. 


Displacement Experiment 


The overall area utilized by a nudibranch within a 
hydroid colony was generally not affected by additions of 


W. J. Lambert, 1993 Page 119 


Table 1 


Location of nudibranchs in pair-wise manipulative experiments before and after an increase in nudibranch densities. 
Values are means (+SE) of nudibranch height (mm) on hydrocauli and density (mumber/cm?) of hydrocauli around a 
nudibranch. Treatment designations (A, B) refer to the identity and order of introduction of nudibranch species. (d.f. = 


degrees of freedom; NS = not significant.) 


Treat- Height Density 
ment d.f. Before After P d.f. Before After P 
Tergipes : Dendronotus 
AA 1,33 6.1 5.4 NS 1,33 9.3 6.4 0.001 
(+1.0) (GE ilSib) (+0.6) (+0.4) 
AB 1,23 U2 8.4 NS 1,23 10.1 8.7 NS 
(+1.6) (Gee5)) (+0.8) (+0.7) 
BA 1,4 0.0 0.0 NS 1,4 9.0 9.0 NS 
(+0.6) (+0.6) 
BB Lia 0.0 0.2 NS 1,17 9.7 6.2 0.002 
(+0.2) (2155) (+0.3) 
Dendronotus : Doto 
AA 1,34 1.7 2.1 NS 1,34 6.5 6.3 NS 
(+0.9) (+0.8) (+0.4) (+0.5) 
AB 2a 2.6 2.3 NS 12 6.2 557 NS 
(Gane3)) (Geile) (+0.5) (+0.4) 
BA 1,16 0.0 0.0 NS 1,16 6.7 6.0 NS 
(+0.3) (+1.2) 
BB 1-23 0.0 0.4 NS 1,23 6.3 4.4 0.010 
(+0.3) (+1.5) (+0.2) 
Tergipes : Doto 
AA 1,26 53) 6.8 NS 1,41 6.1 5.0 NS 
Ge2 1) (Eis) (+0.3) (+0.3) 
AB 1,37 4.3 6.9 NS 1,36 6.3 5.6 NS 
(+0.7) (GEA) (+0.4) (+0.5) 
BA 1,22 0.0 2.9 NS 1,22 6.3 4.7 NS 
(+2.9) (+0.9) (+1.2) 
BB 1,23} 0.0 0.7 NS 1,23 Be 7.0 NS 
(+0.5) (+0.3) (+0.6) 
Doto : Eubranchus 
AA 1,19 13} 0.0 NS 1,19 4.8 WED; 0.030 
(+1.3) (+1.0) (+0.5) 
AB 1,14 4.9 1.2 NS 1,14 5.3 7.4 NS 
(+3.5) (+1.2) (+1.0) (+1.1) 
BA 1,8 7.8 4.8 NS 1,8 6.4 6.7 NS 
Gaal) (+0.8) (+0.8) (+0.7) 
BB Mts 3.0 0.5 NS 1,11 6.1 5.2 NS 
(+1.3) (+0.5) (+0.5) (+0.7) 


heterospecifics or conspecifics. Positional height within the 
colony did not vary significantly in any of the four treat- 
ments (Table 1). 

The area occupied by a nudibranch changed with respect 
to the density of hydrocauli in intraspecific trials only 
(Table 1). Nudibranchs generally moved to areas of the 
colony where the density of hydrocauli was less. The pat- 
tern of change was inconsistent among treatments for Den- 
dronotus frondosus and Doto coronata. Dendronotus frondosus 
moved to an area of fewer hydrocauli in one treatment, 
but remained in an area with similar density in the other. 
Doto coronata moved to areas of higher and lower density 
and also remained among hydrocauli of similar densities, 


after an addition of nudibranchs. There was no change in 
the density of hydrocauli around Eubranchus exiguus after 
an addition of nudibranchs. Tergipes tergipes moved to 
areas with fewer hydrocauli after conspecifics were added 
to the hydroid colonies (Table 1). 

Individual spacing between conspecifics did not vary 
among treatments (Table 2). Individuals of Dendronotus 
frondosus, Doto coronata, and Tergipes tergipes maintained 
a similar distance from conspecifics regardless of the iden- 
tity of the other nudibranch species present. Within each 
treatment involving these three species, inter- and intra- 
specific distances were similar for each of the species of 
nudibranch (Table 2, Treatment 1, 2, 3). Spacing between 


Page 120 


The Veliger, Vol. 36, No. 2 


Table 2 


Summary of patterns of spacing in interspecific associations of nudibranchs on colonies of Obelia geniculata. Values are 
mean distances (mm) between any two nearest neighbors. (* Distances between individuals from monospecific trials.) 


Treatment Species A Species B 
Ie Tergipes Tergipes 
Tergipes Dendronotus 
* Dendronotus Dendronotus 
2 Tergipes Tergipes 
Tergipes Doto 
*Doto Doto 
3% Dendronotus Dendronotus 
Dendronotus Doto 
*Doto Doto 
4. a. Doto Doto 
b. Doto Eubranchus 
c. Eubranchus Eubrarchus 


individuals of Doto coronata and Eubranchus exiguus dif- 
fered (Table 2, Treatment 4). Individuals of Doto coronata 
were closer to each other than to E. exiguus, but distances 
between individuals of E. exiguus did not differ from in- 
terspecific distances with Doto coronata. 

Nearest neighbor analysis (CLARK & EVANS, 1954) was 
used to determine the pattern of dispersion among con- 
specifics for the four species of nudibranchs. At average 
field densities, Dendronotus frondosus and Tergipes tergipes 
were distributed regularly, and Doto coronata and Eubran- 
chus exiguus were randomly distributed throughout the 
hydroid colony (Table 3). The pattern of dispersion changed 
only when densities of Doto coronata were increased; Doto 
coronata tended to aggregate (clump) at higher densities. 
Patterns of dispersion did not change when densities of 
Doto frondosus, E. exiguus and T. tergipes were increased. 


DISCUSSION 


Behavioral encounters between any two nudibranchs oc- 
curred frequently, but aggressive encounters were rare and 
interactions did not influence the microhabitat utilized or 
the location where a nudibranch fed. Individual spacing 
between conspecifics was not generally altered at increased 
densities. ZACK (1976) described the behavioral patterns 
during encounters between pairs of Hermissenda crassicor- 
nis (Eschscholtz, 1831). The vast majority of these behav- 
ioral encounters were non-aggressive and involved two 
animals making contact, touching briefly, and withdraw- 
ing. He found no evidence of aggression or territoriality 
in field populations, although he hypothesized that ago- 
nistic behaviors serve to distribute animals over the sub- 
strate or to ensure access to food. Also, Facelina bostoniensis 
(Couthouy) feeds upon other nudibranchs and possibly 
conspecifics (personal observations; Todd, personal com- 
munication). Although these aggressive interactions may 


Distance (mm) 


between 

individuals 

(+SE) n P 
14.2 (+2.2) 22 NS 
16.2 (+4.0) 11 
10.2 (+1.8) 16 
10.5 (+1.1) 40 NS 
11.8 (+4.0) 13 

6.7 (£1.9) 22 
Ie (GETEG) 27 NS 
AGEs) 8 

7.8 (+1.7) 22 

6.4 (+2.9) 6 a:b 0.027 
15.1 (#2.1) 13 
ZAOKGES 8 b:c NS 


disperse nudibranchs throughout a hydroid colony and 
possibly reduce competition, this is not apparent for the 
nudibranchs in Obelia geniculata. 

Many ecological patterns are attributed to competition, 
but alternative hypotheses should be explored and assessed 
(LAWTON & STRONG, 1981). Interspecific competition has 
been designated the cause of niche separation, character 
displacement, and density compensation (SCHOENER, 1982; 
Copy & DIAMOND, 1975). However, despite the apparent 
lack of competition for food, the feeding behaviors of these 
four Gulf of Maine nudibranchs differ (LAMBERT, 1991a). 
LAWTON & STRONG (1981) stress that the important ques- 
tion to ask is not whether differences exist between species, 
but are the differences greater than other factors dictate? 

A primary reason for rejecting interspecific competition 
as a major structuring force in this instance is the lack of 
intraspecific competition (MILLER, 1967; Morse, 1980; 
STRONG et al., 1984; KEDDy, 1989). Behavioral interac- 
tions between conspecifics were primarily non-aggressive 
(81%) (Figures 1-4) and at times resulted in the two nu- 
dibranchs mating. 

Displacement from a feeding position was not observed 
and the dispersion of nudibranchs within the hydroid col- 
ony was altered by increased densities of conspecifics for 
one species; in this instance individuals aggregated. Two 
hypotheses are suggested to account for these observations. 
First, food resources are not limiting. Many researchers 
have inferred that nudibranchs exert ecologically impor- 
tant impacts on fouling communities by consuming par- 
ticular hydroid prey (CLARK, 1975; Harris, 1987; TopD 
& HAVENHAND, 1989), but no work has yet experimentally 
demonstrated that food is limiting to these nudibranchs. 
Although CLARK (1975) shows an inverse relationship be- 
tween egg production and predation index for Catriona 
aurantia (Winckworth) on colonies of Tubularia spp. that 


W. J. Lambert, 1993 


Page 121 


Table 3 


Patterns of intraspecific dispersion of nudibranch species on colonies of Obelia geniculata. Designations of “before” and 

“after” refer to an addition of individuals to manipulate densities of nudibranchs in pair-wise experiments. Patterns of 

dispersion (R) were determined by methods described in CLARK & EvANS (1954). (R = the degree the observed distance 
departs from a random expectation (R = 1).) 


Mean distance (mm) 
between individuals (+SE) 


Species n Before n After 
Dendronotus 6 1383 t 13.0 
(+1.8) (+2.1) 
Doto 2 11.2 5 2E5 
(#1.5) (+0.9) 
Eubranchus 3 12.2 5 10.4 
(+4.9) (+0.4) 
Tergipes if 14.1 8 13.3 
(+1.9) (+1.8) 


Pattern of dispersion 


Before After 

R P R P 
1.48 0.04 1.56 0.02 
(regular) (regular) 
0.72 NS 0.25 0.02 
(random) (clumped) 
0.96 NS 1.05 NS 
(random) (random) 
1.69 0.01 1.71 0.004 
(regular) (regular) 


suggests fecundity decreases when nudibranchs are present 
at high densities, most hydroid-eating nudibranchs are 
opportunistic, fugitive species with short life-spans and a 
single reproductive period just prior to death (Topp, 1981, 
1983). Thus by the time a hydroid colony is eliminated, 
nudibranchs within the colony may well have concluded 
reproduction and begun to undergo senescence. Second, 
nudibranchs within the hydroid colony are generally in- 
different to each other’s presence. Nudibranchs contacted 
each other only while crawling within hydroid colonies. 
The majority of these interactions was non-aggressive and 
recognition of other nudibranchs by a mechanism other 
than tactile contact was rare. 

Variable recruitment may function to regulate com- 
munities and reduce competition (CREESE & UNDERWOOD, 
1982; QUINN & RyAN, 1989). Although these four nudi- 
branchs have similar recruitment patterns (LAMBERT, 
1991b) with peaks in colonization occurring during the 
summer months when food is plentiful and alternative 
foods are available (personal observations; Kuzirian, un- 
published data), their abundance patterns vary between 
years, suggesting non-equilibrial patterns of coexistence 
(LAMBERT, 1991b). Obelia geniculata also grows epiphyt- 
ically on Agarum cribrosum (Mertens) Bory and there are 
other common thecate hydroids on rocky substrate (per- 
sonal observations). These represent potential alternative 
habitats and food resources for settling veligers that would 
reduce competitive interactions and promote coexistence. 
Also, CLARK (1975) speculated that competent veligers of 
Cratena pilata (Gould) may discriminate among potential 
settling sites that are occupied by competitors to decrease 
interactions (see also, GROSBERG, 1982). 

Predation by the wrasse Tautogolabrus adspersus (Wal- 
baum), which is a visual, epibenthic predator, may regulate 
the nudibranch populations and also facilitate coexistence 
of the nudibranchs. The majority (82.6%) of nudibranchs 
inhabiting Obelia geniculata colonies are less than 3 mm 


in length (LAMBERT, 1990). These animals are immature 
(SWENNEN, 1961; MILLER, 1962; ROBILLIARD, 1970) and 
apparently cryptic. It is likely that as nudibranchs grow 
they are more susceptible to fish predation by 7. adspersus 
because this teleost readily eats nudibranchs both in the 
laboratory (HARRIS, 1986; unpublished data) and in the 
field (personal observations). Large nudibranchs are more 
likely to be encountered and eaten by fish non-specifically 
grazing the hydroid colonies. 

Nudibranchs associated with Obelia geniculata have dif- 
ferent radulae and feed by different mechanisms (LAM- 
BERT, 1991a). Dietary specialization has been suggested 
to alleviate competition for a number of gastropod species 
(NYBAKKEN & EASTMAN, 1977; BLINN et al., 1989; HAaw- 
KINS et al., 1989; MAZZELLA & Russo, 1989). Also, shifting 
to other prey species can reduce competition by decreasing 
feeding pressure in the habitat where veligers are most 
likely to settle. Dendronotus frondosus exploits O. geniculata 
probably only as juveniles and feeds on the hydroids Tubu- 
laria spp. when larger (>10 mm) (SWENNEN, 1961). 
THOMPSON & Brown (1984) and Kuzirian (unpublished 
data) state that Doto coronata feeds on other hydroids as 
adults. The majority of Doto coronata found on the hydroid 
Thuiaria argentea (L.) was greater than 3 mm over 4 years 
(1972-1975) (Kuzirian, unpublished data) whereas 71.37% 
of Doto coronata in Obelia geniculata was less than 3 mm 
(LAMBERT, 1990). 

Selection of specific sites to live within a larger area 
may allow coexistence (BIRCH, 1979; FLETCHER & 
UNDERWOOD, 1987; MazZELLA & Russo, 1989). Nudi- 
branchs use different areas within Obelia geniculata colo- 
nies (LAMBERT, 1991a). Dendronotus frondosus is found 
throughout the colony on hydrocauli, but is present only 
when small (<5 mm). Doto coronata occupies the edges of 
the colony on the kelp surface. Eubranchus exiguus exists 
also at the edges of the colony, but mainly on hydrocauli. 
Tergipes tergipes is generally located in the center of O. 


Page 122 


geniculata colonies atop the hydrocauli. Thus 7. tergipes 
is further specialized in its use of the hydroid colony in 
occupying a third dimension; the other three nudibranchs 
are two-dimensional specialists. 

A low diversity of nudibranch species is present in the 
northwest Atlantic compared to the northeastern Pacific 
and British Isles (Marcus, 1961; FRANz, 1970; Topp, 
1981). CLARK (1975) suggested that “climatic stability” 
with respect to biogeographical patterns of species is the 
primary reason for the low diversity in the northwestern 
Atlantic because annual variation in the water tempera- 
tures may be >20°C. He proposed that these climatic 
effects could influence the degree of competition and be- 
havioral interactions among co-occurring nudibranchs. In 
southern New England CLARK (1975) recorded the co- 
occurrence of Cratena pilata, Tergipes tergipes, and Tenellia 
fuscata (Gould) on Obelia geniculata and suggested that 
rising water temperatures influence competition by elim- 
inating a competitor from a community. Thus a temporal 
separation of nudibranch populations might occur via dif- 
ferences in thermal tolerance of the respective species. 

GERHART (1986) suggested that colonial marine inver- 
tebrates and their gastropod predators have important par- 
allels to terrestrial plant-herbivore communities. In each 
system the prey have a large capacity to regenerate lost 
parts, and consumers are partial predators (HARVELL, 1984) 
capable of sequestering components of the prey for their 
defense (EDMUNDS, 1966; RHOADES & CATES, 1976). The 
roles of nudibranchs in this hydroid community appear 
analogous to those of leaf-eating and tissue-sucking insects 
on plants. In particular, although differences in feeding 
structures and microhabitat selection could mediate com- 
munity structure (HAJEK & DAHLSTEN, 1986; LAMBERT, 
1991a), the apparent lack of a limiting resource and the 
absence of aggressive interactions among individuals (ROOT, 
1973; Zack, 1976; SIMBERLOFF, 1978; LAWTON, 1982; 
STRONG, 1982; this study) suggest that competition is un- 
important in these communities (see review, STRONG et al., 
1984). Future considerations of this parallel may provide 
new insights and generalizations on the evolution of pred- 
ator-prey systems. 


ACKNOWLEDGMENTS 


The manuscript was improved by comments from A. Ku- 
zirian, A. Marsh, M. Litvaitis, J. Berman, L. Harris, J. 
Haney, R. Karlson, Y.-S. Kiang, C. Todd, K. Clark, and 
an anonymous reviewer. A. Kuzirian also provided access 
to dive logs and unpublished data on patterns of nudi- 
branch abundances. I thank P. Levin for diving assistance 
and J. Taylor for statistical advice. Thanks also to H. 
Howell for providing space at the Coastal Marine Lab. 
Financial assistance was provided by a Dissertation Fel- 
lowship from the University of New Hampshire, Graduate 
School. This paper is part of a dissertation submitted in 
partial fulfillment of the requirements for a Ph.D. in Zo- 
ology at the University of New Hampshire. 


The Veliger, Vol. 36, No. 2 


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The Veliger 36(2):124-133 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Redescription and ‘Taxonomic Reappraisal of the 


Tropical Indo-Pacific Nudibranch Siraius nucleola 
(Pease, 1860) (Anthobranchia: Doridoidea: Dorididae) 


GILIANNE D. BRODIE 


Department of Marine Biology, James Cook University of North Queensland, 
Townsville, Queensland, Australia 4811 


RICHARD C. WILLAN 


Northern Territory Museum of Arts and Sciences, G.P.O. Box 4646, 
Darwin, Northern Territory, Australia 0801 


Abstract. Siraius nucleola (Pease, 1860) is widespread in the tropical Indo-Pacific Ocean. Material 
for this paper comes from coastal and oceanic (?.e., Norfolk Island) Australian waters, where the species 
is common but previously unrecorded. A description of external and internal morphology is presented, 
not only for reconciling intraspecific variation in our material with that described in the literature, but 
also for separating generic and specific characters which are confused in previous accounts. Minor 
inconsistencies in body pigmentation, rhinophores, and gills not attributable to intraspecific variation 
are indicative of differing interpretations rather than of different species. Doriorbis Kay & Young is 
synonymized with Szrazus Er. Marcus. As redefined on rhinophoral and radular characters, Siraius is 
enlarged to accommodate five species worldwide—S. bicolor (Bergh, 1884), S. fretterae (Thompson, 
1980), S. zo Er. Marcus, 1955, S. kyolis Ev. & Er. Marcus, 1967, and S. nucleola (Pease, 1860). 


INTRODUCTION 


The genus Doriorbis was erected by Kay & YOUNG (1969) 
for the small dorid nudibranch described by PEASE (1860) 
as Doris nucleola. The principal characters used by Kay 
& YOUNG (1969) to diagnose the genus were: simple pin- 
nate gills forming a circle about the anus; gills retractile 
into a circular sheath; radular teeth simple except for the 
6-8 “outer lateral” (z.e., marginal) ones which bear small, 
apical (7.e., pectinate) denticles; Y- or T-shaped, yellow, 
medial streak extending from the rhinophores to the mid- 
dorsum. We now recognize that these characters are a 
mixture of generic and specific ones, so there is a need to 
separate them for the benefit of future workers investi- 
gating taxonomy or phylogeny in the Dorididae. 
Twenty-four specimens of Szraius nucleola have been 
recorded along the coast of Australia since 1959. Eight of 


the 20 animals discovered in Queensland were collected 
for this study. Four were dissected and the remaining four, 
all from Statue Bay, Yeppoon, have been deposited intact 
in the Museum of Tropical Queensland (formerly Queens- 
land Museum [North Queensland Branch]), Townsville, 
under the registration number MO17432. A further nine 
specimens were collected at Norfolk Island in the Tasman 
Sea off Australia’s east coast during the course of this 
investigation. 


TAXONOMY 
Order Nudibranchia Blainville, 1814 
Suborder Anthobranchia Férussac, 1819 
Superfamily DoriIpoIDEA Odhner, 1934 


Family DoORIDIDAE Rafinesque, 1815 


G. D. Brodie & R. C. Willan, 1993 


Page 125 


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Figure 1 


Straius nucleola. Specimen photographed live; length 14 mm. From intertidal zone, Statue Bay, Yeppoon, central 
Queensland, Australia, 16 June 1988. Photograph: Jon Brodie. 


Genus Siraius Er. Marcus, 1955 
Siraius nucleola (Pease, 1860) 


(Figures 1-17) 


Synonymy 


Doris nucleola PEASE, 1860:29, no. 31; ABRAHAM, 1877:211, 
Doris species 148; BERGH, 1881:pl. G, figs. 10, 11; PRU- 
VOT-FOL, 1947:108. 

Doris papillosa PEASE, 1860:30, no. 34; PRUVOT-FOL, 1947: 
108 (misidentification, not Doris papillosa Muller, 1776, 
or Doris papillosa Kelaart, 1858). 

Doris tincta PEASE, 1864:510 (replacement name for Doris 
papillosa Pease, 1860). 

Doris carinata ALDER & HANCOCK, 1864:122, pl. 29, figs 5, 
6 (misidentification, not Doris carinata Quoy & Gai- 
mard, 1832). 

Doris carina ABRAHAM, 1877:209, Doris species 122 (replace- 
ment name for Doris carinata Alder & Hancock, 1864). 

Doris papillata [sic = error pro papillosa| Pease: ABRAHAM, 
1877:211, Doris species 147. 

Platydoris immonda RISBEC, 1928:84, pl. 1, fig. 4, text fig. 
12; RisBec, 1953:30. 

Doriorbis nucleola (Pease): YOUNG, 1969:423; Kay & YOUNG, 
1969:178, 179; Kay, 1979:458, fig. 148A. 

Halgerda rubicunda Baba: ORR, 1981:43 (misidentification, 
not Halgerda rubicunda Baba, 1949). 


No complete synonymy has been presented before. Kay 
& YOUNG (1969) laid the foundations when they concluded 
the names Doris nucleola Pease, 1860, and D. papillosa 
Pease, 1860 (= D. tincta Pease, 1864) were synonymous 
and, acting as first revisers, selected D. nucleola as the name 


for this species. At the same time they created the new 
generic name Doriorbis. ABRAHAM (1877) had realized much 
earlier that D. carinata Alder & Hancock, 1864, was pre- 
occupied by D. carinata Quoy & Gaimard, 1832, but in 
creating the replacement name, D. carina, Abraham only 
added another junior synonym. RISBEC’s (1928) name 
Platydoris immonda is a further synonym. We are confident 
of this from the description of body coloration and mantle 
ornamentation. RISBEC (1953:30) himself indicated that P. 
immonda might be the same as D. carinata Alder & Han- 
cock. 

References to this species since RISBEC (1953) have failed 
to present the entire synonymy (Kay & YOUNG, 1969; 
YOUNG, 1969; ORR, 1981), so we have done so for com- 
pleteness. 

Doris nucleola possesses no generic character that might 
exclude it from Siraius. As stated above, KAY & YOUNG 
(1969) created the genus Doriorbis solely for D. nucleola 
Pease and they did not mention Szrazus. Had they been 
aware of that genus, they would almost certainly have 
opted to include D. nucleola in it. Actually, R. Burn rec- 
ognized the synonymy of Doriorbis and Siraius some 15 
years ago (Burn, personal communication, 1991). 

Since Stratus is not a Latin or Greek word and ER. 
Marcus (1955) gave no etymology, we take its gender to 
be masculine. Further, we interpret the specific name nu- 
cleola, which is derived from a Latin word meaning a “‘little 
nut” or “kernel,” as a noun in apposition and accordingly 
its termination will not change to -us to agree with the 
gender of the genus. Therefore the correct combination is 
Siraius nucleola. 


Page 126 The Veliger, Vol. 36, No. 2 


2 RSC AS a) t Uae 
Explanation of Figures 2 to 7 
Figures 2-7. External morphology of Szrazus nucleola. 


Figure 2. Lengths 13, 11 mm. From low tide, “The Strand,” Cleveland Bay, Townsville, northern Queensland, 
20 March 1989. Photograph: R. C. Willan. 


Figure 3. Length 21 mm. From 12 m, northern side of North West Solitary Island, northern New South Wales, 
6 April 1991; note that rhinophores are retracted. Photograph: R. Gentle. 


Figure 4. Length not recorded. From low tide, Statue Bay, Yeppoon, central Queensland, 16 June 1988. Spawn 
mass on right. Photograph: J. Brodie. 


Figure 5. SEM of whole animal, length 12 mm. From low tide, “The Strand,” Cleveland Bay, Townsville, northern 
Queensland, 8 March 1988. Bar = 1 mm. 


Figure 6. SEM showing detail of right rhinophore and ornamentation on surrounding mantle of specimen depicted 
in Figure 5. Bar = 0.5 mm. 


Figure 7. SEM showing detail of extended gills of specimen depicted in Figure 5. Bar = 1 mm. 


G. D. Brodie & R. C. Willan, 1993 Page 127 


Explanation of Figures 8 to 13 


Figures 8-13. Radula of Straius nucleola. Bar = 10 wm in all figures. 
Figure 8. SEM of inner face of two inner lateral teeth (approximately row 6, teeth numbers 5 and 6). 
Figure 9. SEM of one row (number 20 approximately) of outer lateral teeth showing outer faces. 


Figure 10. SEM of same row as in Figure 9 showing detail of outer faces of two outer lateral teeth; note denticles 
at base of cusp. 


Figure 11. SEM of one row (number 30 approximately) of outer lateral teeth showing inner faces; note absence 
of denticles at base of cusp. 


Figure 12. SEM of outermost lateral (above) and marginal teeth (below) of two rows (numbers 18 and 19 
approximately) showing outer faces. 


Figure 13. SEM showing detail of most marginal tooth; note apical fringe of minute denticles. 


The Veliger, Vol. 36, No. 2 


Page 128 


Material Examined 


In the following list, locations on the Australian coast 
are given first. They are arranged counterclockwise start- 
ing with the southeasternmost one. The Norfolk Island 
localities then follow with the same arrangement. Mea- 
surements are those of animals in the extended crawling 
state. 

AUSTRALIA: 1 specimen (21 mm), 12 m, northern side 
of North West Solitary Island, northern New South Wales 
(30°01'S, 153°16’E), B. Morgan, 6 April 1991 (color trans- 
parency only available for examination); 1 specimen (12.5 
mm), intertidal, Angourie Pool, northern New South Wales 
(29°29'S, 153°21'E), R. Burn, 3 October 1959 (National 
Museum of Victoria, Reg. No. F27396); 11 specimens (2- 
14 mm), intertidal, Statue Bay, Yeppoon, Queensland 
(23°10’S, 150°47’E), G. & J. Brodie, 27 March 1988; 4 
specimens, intertidal, Statue Bay, Yeppoon, Queensland 
(23°10'S, 150°47’E), J. Brodie, 22 May 1988; 2 specimens, 
intertidal, Statue Bay, Yeppoon, Queensland (23°10’S, 
150°47'E), J. Brodie, 16 June 1988; 1 specimen, intertidal, 
Putney Beach, Great Keppel Island, Queensland (23°10’S, 
150°58’E), J. Brodie, 10 April 1988; 2 specimens (13, 11 
mm), intertidal, ““The Strand,” Cleveland Bay, Towns- 
ville, Queensland (19°15’S, 146°49’E), G. Brodie, 8 March 
1989; 1 specimen, 4.5 m, Bundegi Reef, Exmouth Gulf, 
central Western Australia (21°51’S, 114°10'E), N. Cole- 
man, 27 August 1972 (color transparency only available 
for examination). 

NORFOLK ISLAND (29°01'S, 167°59’E): 1 specimen (7 
mm), 11 m, Ball Bay, S.E. coast of Norfolk Island, D. & 
R. Gentle, November 1991; 1 specimen (11 mm), 6 m, 
“The Fireplace,” Duncombe Bay, N.W. coast of Norfolk 
Island, D. & R. Gentle, November 1991; 1 specimen (13 
mm), 12 m, offshore from “Crystal Pool,” S.W. coast of 
Norfolk Island, K. Whysall & R. C. Willan, 16 March 
1992; 1 specimen (3 mm) with bifurcated left rhinophore, 
3m, Slaughter Bay, S. coast of Norfolk Island, K. Whysall, 
February 1992; 2 specimens (10, 6 mm), 15 m, “Coral 
Garden,” N.E. tip of Nepean Island, just south of Norfolk 
Island, D. & R. Gentle, November 1991; 1 specimen (11 
mm), 15 m, Spin Bay, S.E. coast of Phillip Island, south 
of Norfolk Island, K. Whysall & R. C. Willan, 17 March 
1992; 2 specimens (10, 10 mm), 14 m, Sail Rock, northern 
coast of Phillip Island, south of Norfolk Island, K. Why- 
sall, November 1991. 


Description 


Maximum length is 21 mm, though 10-13 mm is more 
usual for adults. In life (Figures 1-4), the body of Siraius 
nucleola is elongate-ovate and flatly convex in profile. Al- 
though the mantle appears smooth at first glance, it ac- 
tually possesses numerous, rounded pustules. The mantle, 
which covers the foot at all times, even posteriorly, is firm 
and feels rough because of a dense subepidermal layer of 
spicules. In addition to the pustules, a few taller papillae 
are present along the dorsal midline (Figure 5). Neither 


body shape, nor the dimensions of the pustules/papillae 
are altered by preservation. 

The rhinophores are relatively large and fully retractile. 
The clavus is elongate with widely spaced lamellae and a 
blunt apex. Both of the two specimens (14 and 10 mm) 
from Statue Bay, Queensland, had 10 lamellae on the right 
clavus. The rhinophoral pockets possess 5 to 7 upstanding 
papillae around their rim (Figure 6). These papillae are 
not all the same size; the 2 lateral ones are considerably 
larger than the rest. 

The 5 gills, shown extended in Figure 7, are tripinnate. 

The group of 11 specimens observed at Statue Bay on 
27 March 1988 possessed either dull yellow-orange or dark 
tan or dark green mantles. Besides these colors, other spec- 
imens from Australia had khaki, orange, dirty yellow, or 
blue-black mantles. Every specimen had a dull orange- 
yellow mantle undersurface and foot sole. A sprinkling of 
granules imparted a brown coloration to the apices of the 
pustules on the mantle. A pale hourglass-shaped patch 
extended mid-dorsally from between the rhinophores to 
just in front of the gills. This patch can be interrupted or 
less pronounced in small specimens. It was opaque white 
or light brown, consistently paler than the mantle, and it 
sometimes had a narrow, purplish brown marginal zone. 
After preservation, the patch retained a faint violet hue. 
In all specimens, the rhinophores bore a cream base and 
dirty brown to black clavus which, like the dorsal patch, 
sometimes displayed a purplish tinge. The gills were uni- 
formly brown, and consistently paler than the mantle. 

The specimen from North West Solitary Island (Figure 
3) was unusual in lacking the mid-central cream streak 
on the mantle, so that the transverse markings (the top 
and base of the “‘hourglass”) behind the rhinophores and 
in front of the gills were disconnected. Its gills, which were 
broader than those possessed by other specimens, had 
opaque white bases and dark purple-brown extremities. 
Its gills and the mantle were peppered with numerous, 
microscopic, opaque white spots. 

When the mantle is opened dorsally, the internal organs 
are clearly visible through the unpigmented walls of the 
thin, ensheathing visceral envelope. A composite view of 
the digestive system is given in Figure 14 and a more 
detailed view of the connections within the lumen of the 
digestive gland (7.e., the openings to the oesophagus, cae- 
cum, and stomach) is given in Figure 15. The oral tube 
is relatively short and conical, and its junction with the 
pharyngeal bulb is marked by a circle of small extrinsic 
oral retractor muscles. A single, large extrinsic buccal re- 
tractor muscle is present on either side of the pharyngeal 
bulb ventrolaterally. A small radular sac lies beneath the 
expanded posterior half of the pharyngeal bulb. The paired 
salivary glands are tubular, flattened, and exceptionally 
long; each is connected to the posterior of the pharyngeal 
bulb by a narrow duct. These glands extend side by side 
beneath the oesophagus, the apex of each being tethered 
to the undersurface of the digestive gland by a thread of 
connective tissue. The oesophagus has a dilation just in 


G. D. Brodie & R. C. Willan, 1993 


Page 129 


qe 


Explanation of Tene me to 16 


Figures 14-16. Gut and radula of Szraius nucleola. 


Figure 14. Composite view of structure of alimentary canal. Abbreviations: a.p., anal papilla; ca., caecum; d.g., 
digestive gland; int., intestine; oes., oesophagus; o.t., oral tube; r., rectum; r.sa., radular sac; s.g., salivary gland; st., 


stomach. Bar = 1 mm. 


Figure 15. Detail of midgut; digestive gland partially removed to reveal interconnections of oesophagus, stomach, 
caecum, digestive gland, and intestine. Abbreviations: ca., caecum; d.g., digestive gland; d.l., cut wall of digestive 
gland; du., openings from digestive gland; int., intestine; oes., oesophagus; st., stomach. Bar = 1 mm. 


Figure 16. Radula. a. Innermost lateral teeth, row 3, dorsal view. b. Inner lateral teeth, row 4, profile. c. Teeth 7 
and 8, row 11. d. Outer lateral teeth, row 6, profile. e. Extreme outermost lateral teeth, row 6, profile. 


front of its middle section. Dorsally, the cream-colored 
stomach was observed to be cupped between two anterior 
lobes of the digestive gland. A caecum opens into the lumen 
of the digestive gland below, and just to the left of, the 
common atrium of the oesophagus and stomach (7.e., it is 
not encircled by the intestine). The intestine emerges from 
the stomach on the left side and disappears beneath it for 
a short distance before reappearing just to the right of the 
mid-dorsal line. It then passes over the top of the greenish 


digestive gland (whose surface was covered by the cream 
ovotestis) and continues rearwards to end at the darkly 
pigmented anal papilla. 

After treatment with potassium hydroxide, the pharyn- 
geal bulb yielded a lightly cuticularized labial ring and a 
relatively broad yet elongate radula. There were definitely 
no jaws. Radulae of the 11- and 10-mm specimens from 
Statue Bay measured 1.2 and 1.1 mm long by 1.09 and 
0.7 mm in maximum width, respectively, when spread out 


Page 130 


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The Veliger, Vol. 36, No. 2 


amp. 


imm 


Figure 17 


Straius nucleola. Composite view of structure of reproductive organs of a sexually mature specimen. Abbreviations: 
amp., ampulla; b.c., bursa copulatrix; h.d., hermaphroditic duct; n.g., nidamental glands; ov., oviduct; pr., proximal 
section of vas deferens; r.s., receptaculum seminis; va.d., distal vas deferens. 


and laid flat on microscope slides. Radular formulae were 
34 x 4-40-0-40-4 (14 mm animal), 26 x 3:-34-0-34-3 
(11 mm animal) and 25 x 3-26-0-26-3 (10 mm animal). 

Except for the outermost laterals and marginals, all the 
teeth are simple (7.e., hamate) with flanges posteriorly. In 
the following account, numbers relate to individual teeth 
across one half-row near the growing end of the largest 
(14 mm) Queensland specimen. The innermost laterals 
(Figure 16a) are relatively small with a hooked cusp. Mov- 
ing away from the midline, the laterals become larger and 
their cusps more erect (Figures 9, 16b, c). Nine of the 
outer laterals (tooth numbers 30-38) bear three minute 
denticles at the base of the cusp on the outer face (Figure 
10). Outer lateral number 39 has two denticles (Figure 
12) and outer lateral number 40 has none at all. The 
outermost three or four teeth (the marginals) bear an apical 
fringe of minute, pectinate denticles (Figures 12, 13, 16e). 

A composite view of the unravelled reproductive system 
is presented in Figure 17. The hermaphrodite duct widens 
at about one-third its length into a shiny, white ampulla 
which is relatively elongate. The separation of the distal 
hermaphrodite duct into vas deferens and oviduct takes 
place within the nidamental gland mass. The vas deferens 
maintains its diameter throughout its length, the proximal 
(prostatic) section being tubular and not enlarged. Pre- 
sumably the epithelium in this section is glandular, but 
this was not obvious on dissection and it was not checked 
histologically. No armature could be found on the exterior 
or interior of the simple penis. The vagina is long and 
narrower than the vas deferens with which it is contiguous 


at the genital aperture. The bursa copulatrix and recep- 
taculum seminis, both stalked, arise high up, side by side 
on the vagina (7.e., semiserial arrangement). The bursa is 
spherical and thin walled. The receptaculum is slightly 
smaller than the bursa, ovoid, and thick walled. 

Several egg masses were present alongside the specimens 
from Statue Bay (Figure 4) and these were identical to 
masses laid by captive animals. The masses were firm, 
gelatinous, orange spirals (2.5 to 3.5 whorls), and they 
had a slightly crenulate upper (7.e., free) margin. The lower 
edge (7.e., that attached to the substrate) of whorls was 
separated by gaps of 2 to 3 mm from adjacent whorls. 
There was only a single egg per capsule. The type of larval 
development and the mode of hatching were not recorded. 


Comparison with Previous Descriptions 


Although ALDER & HANCOCK (1864) provided no de- 
tails of the internal anatomy of their Doris carinata, it is 
possible to recognize the species again positively because 
of the colored drawings executed by the Hindu artists 
commissioned by Walter Elliot (ALDER & HANCOCK, 1864: 
pl. 29, figs. 5, 6). The specimens depicted in their drawings, 
which are iconotypes because no actual animals were pre- 
served, had olive green mantles with brown pustules and 
the hourglass-shaped patch on the mantle was pale with 
whitish pustules. 

PEASE’s (1860) specimens from Hawaii had orange (Doris 
nucleola) or grayish (D. papillosa) mantles. We have no 
doubt that our Australian specimens are conspecific with 


G. D. Brodie & R. C. Willan, 1993 


Page 131 


those redescribed as Doriorbis nucleola (Pease) from Ha- 
Wali more than a century later (KAY & YOUNG, 1969). 
Kay & Young’s photograph of a living animal reveals the 
gills to be tripinnate, thus contradicting their description 
of them as “simply pinnate.”’ Other minor differences in- 
volve the number of papillae on the mantle surface (in- 
dicated as “‘a sparse scattering”), the size of the rhinophores 
(indicated as ‘“‘small’’), the blunt (rather than acuminate) 
apex to the rhinophores, and the color of the mid-dorsal 
hourglass-shaped patch (described as “a Y- or T-shaped 
yellow medial streak’’). 

Kay & YOUNG’s (1969) radular description is ambig- 
uous in that it failed to discriminate between outer lateral 
and marginal teeth, and the mention of “small outer den- 
ticles” could relate to either the small basal denticles on 
the outer face of the outer laterals or the apical pectinations 
on the marginal teeth. However, because Kay & Young 
indicate there were 42 teeth across one half-row of the 
radula in their specimen and they illustrate the forty- 
second tooth in their figure 3, we interpret that tooth as 
the outermost marginal and hence the “small outer den- 
ticles” on it must be the apical pectinations. The corollary 
to this conclusion is that either the outer laterals were 
smooth or Kay & Young overlooked them on their spec- 
imen. 

Kay & YOUNG’s (1969) excellent diagram of the repro- 
ductive tract reveals an identical arrangement to that of 
our specimens, even to the connection of the hermaphrodite 
duct/vas deferens/oviduct within the nidamental gland 
mass. On no occasion have we observed the conglobating 
behavior (z.e., rolling into a ball) mentioned by Kay & 
YOUNG (1969) as characteristic of Doriorbis nucleola when 
disturbed. 


Discussion 


ER. Marcus (1955:134) defined Straius on the basis of 
its simple lateral teeth, pectinate marginal teeth, short and 
grooved oral tentacles, short and broad salivary glands, 
tubular (as against enlarged) prostatic region of the prox- 
imal vas deferens, unarmed and protrusible distal vas def- 
erens, lack of penial papilla, and semiserial arrangement 
of allosperm vesicles. He specifically excluded branchial 
and labial characters from his definition of Szraius because 
he believed they had no generic importance (ER. MARCUS, 
1955:135). Later, Ev. & Er. MARCUS (1967:66) dismissed 
the shape of the salivary glands as a generic character 
because of the apparent differences between the three spe- 
cies they had examined (ER. Marcus, 1955; Ev. & ER. 
Marcus, 1967). 

Kay & YOUNG (1969:178) singled out only three char- 
acters which they considered as “most important” for di- 
agnosing Dororbis: “(1) simply pinnate branchiae ar- 
ranged as a circlet about a posterior, mid-dorsal anus and 
retractile into a circular sheath; (2) hamate lateral teeth 
with outermost laterals denticulate; (3) a Y- or T-shaped 


yellow medial streak extending from the rhinophores to 
the mid-dorsum.” Having re-examined the type species 
Doriorbis nucleola, we are now in a position to reappraise 
these three and other characters used to define Doriorbis 
and other related, jawless, caecate, cryptobranch dorids 
(Doris, Etidoris, Stratus, Austrodoris, Alloiodoris, Artachaea). 
The branchial form (which we call tripinnate) occurs in 
most other genera in this close-knit group, so it is not 
diagnostic. Nor, incidentally, are the character states of 
distal vas deferens, penis, and allosperm vesicles for the 
same reason. As clarified above, the radular configuration, 
especially the pectinate marginal teeth, is unique to only 
two genera within this group—S?raius and Etidoris. The 
color pattern is diagnostic of S. nucleola alone. 

In our definition of Szraius (see below) we incorporate 
the state of the rhinophoral pocket (with papillae of un- 
equal size around the margin) because that state occurs in 
four species—Svraius bicolor, §. ilo, S. kyolis, and S. nucleola. 

Our redefinition of Siraius Er. Marcus (with autapo- 
morphies and apomorphic traits in italics) is as follows. 
Small (to 30 mm crawling length), cryptobranch dorids 
with firm mantles supported by non-emergent spicules; 
mantle ornamented with low, scattered, spiculose tubercles 
(and sometimes papillae too); rhinophoral pockets carrying 
papillae of unequal size around rims; gills tripinnate; bran- 
chial pocket usually carrying papillae around rim; oral 
tentacles short and grooved; jaws absent; radula broad, 
lateral teeth simple, marginal teeth pectinate; stomach with 
caecum that rises to surface of digestive gland to left of 
intestine; vas deferens of uniform diameter, proximal 
(prostatic) section tubular and of uniform diameter, distal 
section protrusible—serving as penis and unarmed; bursa 
copulatrix and receptaculum semiserially arranged high 
up on vagina, of equivalent size, both stalked. 

This redefinition of Siraius emphasizes rhinophoral and 
radular features because these are the only characters we 
interpret as derived (or apomorphic in cladistic terminol- 
ogy). Two taxonomically desirable outcomes stem from 
this redefinition. First, it enlarges S:raius to accommodate 
the western Atlantic Doris fretterae Thompson, 1980. The 
only discordant character possessed by that species is its 
smooth branchial pocket, but that state is primitive in the 
group under study and therefore it cannot be used to ex- 
clude the species from the genus. Table 1 compares the 
five species included in Straius according to our definition. 
Second, it allows us to recognize Etidoris and Doriopsis as 
the sister genera to Szraius, because both also possess simple 
tubular prostatic sections of the proximal vas deferens. 
Most species in these three genera possess ribbonlike, flat- 
tened salivary glands (the exception being S. lo Er. Mar- 
cus), equivalent-sized bursa copulatrix and receptaculum 
seminis, and close proximity of these two allosperm vesicles 
to each other on the narrow, straight vagina. The pectinate 
marginal teeth in Szraius and Etidoris indicate these two 
genera are closer to each other than either is to Doriopsis. 
This relationship is strengthened by the highly derived 


The Veliger, Vol. 36, No. 2 


Page 132 


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P e192: 


G. D. Brodie & R. C. Willan, 1993 


branchial configuration of Doriopsis wherein the gill circlet 
is compressed into a rearward-projecting fan overtopped 
by a notal flap. 


Geographic Distribution 


Siraius nucleola is now known from widely separated 
areas of the Pacific Ocean (Hawaii, New Caledonia, Hong 
Kong, Australia, Norfolk Island) and India. We assume 
that it ranges continuously throughout the tropical Indo- 
west Pacific region. 


ACKNOWLEDGMENTS 


Our foremost acknowledgments go to our spouses—Jon 
Brodie and Glynn Maynard—for assistance in many ways. 
Dr. W. L. Ride of the International Commission on Zoo- 
logical Nomenclature gave sound advice on the gender and 
correct formation of the name. Robert Burn kindly sup- 
plied us with his field notes on the specimen of Szraius 
nucleola from Angourie Pool, and we are grateful to him, 
David Brunckhorst, and Leigh Winsor for suggestions to 
improve the manuscript. Reg. Gentle kindly gave permis- 
sion to reproduce his photograph of the unusually colored 
animal from North West Solitary Island. We are most 
grateful to Jon Brodie, Neville Coleman, Reg. and Daph. 
Gentle, and Kevin Whysall for collecting specimens and/ 
or providing color transparencies of Siraius nucleola. 


LITERATURE CITED 


ABRAHAM, P. 1877. Revision of the anthobranchiate nudi- 
branchiate Mollusca, with descriptions or notices of forty- 
one hitherto undescribed species. Proceedings of the Zoo- 
logical Society of London for the year 1877:196-269. 

ALDER, J. & A. HANCOCK. 1864. Notice of a collection of 
nudibranchiate Mollusca made in India by Walter Elliot, 


Page 133 


Esq., with descriptions of several new genera and species. 
Transactions of the Zoological Society of London 5:113-147. 

BeRGH, L. S. R. 1881. Nachtrage. In: C. D. Semper (ed.), 
Reisen im Archipel der Philippinen von Dr. C. Semper, 
Malacologische Untersuchungen 2 (Suppl.) 2:79-128, pls. 
G-L. 

Kay, E. A. 1979. Hawaiian Marine Shells. Reef and Shore 
Fauna of Hawaii. Section 4: Mollusca. Bernice P. Bishop 
Museum: Honolulu. 653 pp. 

Kay, E. A. & D. K. Younc. 1969. The Doridacea (Opistho- 
branchia; Mollusca) of the Hawaiian Islands. Pacific Science 
23:172-231. 

Marcus, ERNST. 1955. Opisthobranchia from Brazil. Boletins 
da Faculdad de Filosofia, Ciéncias e Letras, Universidade 
de Sao Paulo, Brazil, Zoologia 20:89-262, pls. 1-30. 

Marcus, ERNST & EVELINE Marcus. 1970. Opisthobranchs 
from Curagao and faunistically related regions. Studies on 
the Fauna of Curacao and Other Caribbean Islands 33:1- 
129. 

Marcus, EVELINE & ERNST Marcus. 1967. American opis- 
thobranch mollusks. Part I. Tropical American opistho- 
branchs. Studies in Tropical Oceanography 6:i-viii + 137 


PP- 

OrR, J. 1981. Hong Kong Nudibranchs. Urban Council: Hong 
Kong. 82 pp. 

PEASE, W. H. 1860. Descriptions of new species of Mollusca 
from the Sandwich Islands. Proceedings of the Zoological 
Society of London 28:18-36. 

PEASE, W. H. 1864. On errors and omissions in former com- 
munications. Proceedings of the Zoological Society of Lon- 
don for 1863:510. 

PRuvoT-Fo., A. 1947. Les opisthobranches de W. Harper 
Pease. Révision. Journal de Conchyliologie 87:96-114. 
RIsBEC, J. 1928. Contribution a l’etude des Nudibranches Néo- 

Calédoniens. Faune des Colonies Frangaises 2(1):1-328. 

RISBEC, J. 1953. Mollusques nudibranches de la Nouvelle- 
Caléedonie. Faune de l'Union Frangaise 15:189 pp. 

TuHompson, T. E. 1980. Jamaican opisthobranch molluscs II. 
Journal of Molluscan Studies 46:74-99. 

YounG, D. K. 1969. The functional morphology of the feeding 
apparatus of some Indo-West Pacific dorid nudibranchs. 
Malacologia 9:421-445. 


The Veliger 36(2):134-144 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Polygyrid Land Snails, Vespericola (Gastropoda: 


Pulmonata), 1. Species and Populations Formerly 


Referred to Vespericola columbianus 


(Lea) in California 


by 


BARRY ROTH anpb WALTER B. MILLER 


Department of Invertebrate Zoology, Santa Barbara Museum of Natural History, 
Santa Barbara, California 93105, USA 


Abstract. 


Vespericola columbianus pilosus (Henderson, 1928) and V. columbianus orius (Berry, 1933) 


differ from typical Pacific Northwest V. columbianus (Lea, 1838) in shell and reproductive system 
characters and are separated as distinct species. A new species, Vespericola marinensis, is described and 
compared to V. pilosus and V. columbianus. Other California records based on shells of the V. columbianus 


type are summarized. 


INTRODUCTION 


This is the first in a projected series of studies on the 
systematics of the West American polygyrid land snail 
genus Vespericola Pilsbry, 1939. The greatest species di- 
versity occurs in northwestern California and southwestern 
Oregon, where nine species have been named. One addi- 
tional species is described herein. In addition, two species 
formerly regarded as subspecies of Vespericola columbianus 
(Lea, 1838) are shown to differ in genital characters from 
typical V. columbianus and are separated as distinct species. 
The material treated in this and following papers was 
collected by the authors from 1968 to 1991; additional 
material of many of the new taxa was located in museum 
collections. As remarked earlier (ROTH, 1985), the repro- 
ductive system in species of Vespericola is often more strongly 
differentiated than the shell. In many cases, shell char- 
acters are adequate for identification. However, especially 
in the complex of species resembling Vespericola megasoma 
(Pilsbry, 1928), dissection of the mature reproductive sys- 
tem is sometimes necessary for a firm identification. With 
specimens from new localities, it is always desirable to 
establish the species’ identity by dissection. 

Vespericola columbianus pilosus (Henderson, 1928), the 
type species of Vespericola, differs anatomically (and some- 
what in shell characters) from V. columbianus from the 
valley of the Columbia River, Washington-Oregon, and 


accordingly is separated as a distinct species. Its distri- 
bution, limited to central California, is reviewed. Popu- 
lations in Marin County, differing in shell and anatomical 
characters from those on the San Francisco Peninsula, are 
described as a new species, V. marinensis. Vespericola col- 
umbianus orius (Berry, 1933) differs anatomically and con- 
chologically from V. columbianus and is considered a sep- 
arate species. Remaining Californian records based on shells 
of the V. columbianus type (i.e., those in which the inner 
part of the basal lip curves or angles forward in basal view 
and the inner lip is not markedly dilated over the umbil- 
icus) are summarized as a basis for future investigation. 


MATERIALS anD METHODS 


Shell height and diameter are vernier caliper measure- 
ments and exclude the expanded lip of mature shells. Whorls 
were counted by the method of PILsBry (1939:xi, fig. B). 
The density of periostracal setae was estimated by counting 
the number of setae per square millimeter on the shoulder 
of the body whorl, 0.25 whorl behind the aperture of adult 
specimens, at 30 magnification under a dissecting mi- 
croscope with an ocular reticle. Three counts were taken 
per specimen and the mean (to the nearest integer) re- 
corded. 

Specimens for dissection were prepared by the method 
of MILLER (1967). Snails were first drowned in water to 


B. Roth & W. B. Miller, 1993 


Page 135 


insure expansion and relaxation, then heated to a tem- 
perature of 60°C, at which time the bodies could be pulled 
easily from the shells and dissected. After the body cavity 
was opened, the position and maturity of the reproductive 
system were observed; then the whole reproductive system 
was removed, attached to a small patch of body wall around 
the external genital orifice. The penis was slit longitudi- 
nally to expose the verge and the pilasters and papillae on 
the wall of the penial chamber. The verge of at least one 
specimen of every species was completely excised for ex- 
amination. 

Whole mounts of genitalia were prepared by the method 
of MILLER (1967): stained with hematoxylin, dehydrated 
and cleared in successive baths of ethanol and toluene, and 
mounted on slides with Permount mounting medium. Or- 
gan measurements were taken from mounted specimens. 
Anatomical drawings were made by projecting the image 
of the whole mount on paper with an overhead projector. 

Shell growth in Polygyridae is determinate and ends 
with, first, a constriction of the body whorl and then a 
turning outward and thickening of the lip. Reproductive 
maturity normally seems to follow a short time after the 
lip turns, but the presence of a turned lip does not guar- 
antee a reproductively mature specimen. Therefore, at least 
a portion of each sample was kept alive in a terrarium for 
a period of weeks or months before dissection to ensure 
full development of the genital structures. Terraria con- 
sisted of redwood boxes with screened tops. A 3-6 cm layer 
of soil and leafmold from the collecting locality was added. 
Specimens were fed lettuce. There is no indication that 
growth of Vespericola in terraria under these conditions is 
in any way abnormal. 

The following abbreviations are used: ANSP, Academy 
of Natural Sciences of Philadelphia; BR, senior author’s 
collection, San Francisco, California; CAS, California 
Academy of Sciences; LACM, Los Angeles County Mu- 
seum of Natural History; SBMNH, Santa Barbara Mu- 
seum of Natural History; UCM, University of Colorado 
Museum; USNM, United States National Museum of 
Natural History, Smithsonian Institution. 


SYSTEMATICS 
Family POLYGYRIDAE Pilsbry, 1895 
Vespericola Pilsbry, 1939 


Vespericola PILSBRY, 1939:xvii; PILSBRY, 1940:892-894; 
ZILCH, 1960:586. 

Type species: Polygyra columbiana pilosa Henderson, 1928 
[= Vespericola pilosus (Henderson)], by original desig- 
nation. 


Polygyridae with shell small to medium-sized, globose 
to depressed-helicoid, narrowly umbilicate to imperforate. 
Periostracum smooth, matte-surfaced, or granulose, bear- 
ing sparse to densely set setae (or at least their scars). Base 
of last 0.2 turn of body whorl more or less compressed 
upward; strong constriction present behind lip. Parietal 


lamella present or absent (sometimes variably present 
within a species). Lip turned outward and sometimes re- 
flected. No lamellae present on outer or basal lips, but low 
basal callus sometimes present. Epiphallus internally 
ridged, markedly narrower than apex of penis, usually 
with swollen, sausage-shaped upper section, terminating 
in bound, vestigial epiphallic caecum at junction of epi- 
phallus and vas deferens. No penial gland present. Penial 
retractor muscle inserted on epiphallus, distant from penis. 
Retentor muscle originating on epiphallus or branching 
from penial retractor near epiphallus, inserting on summit 
of well developed penial sheath. Upper part of penial 
chamber bearing V-shaped pilasters or diverging rows of 
papillae; or, entire wall of chamber covered with close-set 
papillae. Paired longitudinal pilasters absent. Smooth, con- 
ical, spoon-shaped, or needle-like verge extending forward 
from summit of the penial chamber, containing seminal 
duct, with terminal or subterminal pore, without terminal 
papillae. Much of penis inserted into everted spermathecal 
duct in copulation; basal penis slightly expanded into small 
clasping disk. Verge directed forward during copulation. 

Spider webs, soil, and bits of plant debris often adhere 
among the setae, forming a dark crust; the resulting ap- 
pearance of the shell is cryptic and may mimic a mammal 
dropping. 

The principal species-level diagnostic features of the 
reproductive system are the length of the atrium; the shape 
and dimensions of the penial complex, including the verge; 
the shape and size of the spermatheca (“gametolytic gland,” 
“bursa copulatrix”) and its duct; and the presence or ab- 
sence of a fleshy thickening at or near the base of the 
spermathecal duct. 

EMBERTON (1988, e.g.) does not recognize an epiphallus 
(as distinct from the proximal part of the vas deferens) in 
Triodopsinae. We follow the convention of PILsBRyY (1940) 
and other authors in terming as epiphallus the portion of 
the seminal duct from the insertion of the epiphallic caecum 
(‘“flagellum’’) to the apex of the penis. 

The noun Vespericola is of masculine gender, so adjec- 
tival species names often end in -ws. 

The genus ranges around the northeast Pacific rim from 
the Aleutian Islands to San Luis Obispo County, Califor- 
nia. 

The family-group name Polygyridae Pilsbry, 1895, is 
junior to Mesodontidae Tryon, 1866. A petition to validate 
the better-known name Polygyridae (EMBERTON, 1989) 
has been affirmed (ICZN, 1992). 


Vespericola pilosus (Henderson, 1928) 
(Figures 1-6) 


Polygyra columbiana pilosa HENDERSON, 1928:143; PILSBRY, 
1928:181-182, 185 (in part), figs. 10, 10a; HENDERSON, 
1929:80 (in part; non Alaska and Pacific Northwest 
records, and probably non fig. 35); HENDERSON, 1936: 
255 (reference to California localities only). 

Vespericola columbiana pilosa (Henderson): PILsBRyY, 1939: 


Page 136 


The Veliger, Vol. 36, No. 2 


Explanation of Figures 1 to 3 


Figures 1-3. Vespericola pilosus (Henderson). Shell, BR 1648, CALIFORNIA: San Mateo County: N slope of San 
Bruno Mountain facing Guadalupe Canyon, B. Roth coll., 4 June 1989. Top, apertural, and basal views. Diameter 


13.9 mm. 


xvil; PILSBRY, 1940:896-898 (in part), figs. 513:10, 513: 
10a (non figs. 512C, 512D); INGRAM, 1946:92 (in part); 
INGRAM & LoTz, 1950:25-26 (in part), pl. 5, figs. 5, 6; 
La RocQugE, 1953:309 (in part). 

Vespericola pilosa (Henderson): BAKER, 1962:16. 

Non Vespericola columbiana pilosa (Henderson): WEBB, 1970: 
Po =Tit 

Non Vespericola columbiana var. pilosa (Henderson): 
EYERDAM, 1951:7. 


Diagnosis: A medium-sized Vespericola with depressed- 
helicoid to conical, narrowly umbilicate shell, 5.5-6.3 
whorls, 19-30 periostracal setae/mm?’, and usually no pa- 
rietal lamella. Penis elongate-conical, ratio of protruding 
part to sheathed part approximately 0.87; verge 0.5-0.6 
mm long, conical, ending in 0.1 mm opposing lips. 


Description of shell: Shell medium-sized for the genus 
(diameter 12.3-15.5 mm) depressed-helicoid to conical, 
narrowly umbilicate, with 5.5-6.3 whorls. Spire straight- 
sided or weakly convex; whorls rounded, suture moderately 
impressed. Embryonic whorls 1.5-1.7, with prominent, 
rather coarse, radial wrinkling; wrinkles surmounted by 
smooth, hemispheric to radially elongate papillae. Early 
teleoconch whorls with inconspicuous, crowded, retractive 
growth rugae and irregular granulation with collabral 
trend. Periostracum bearing slender setae in gently de- 
scending rows; setae 19-30/mm/’, approximately 0.2-0.25 
mm long on spire and shoulder of body whorl, erect or 
curving away from direction of coiling, broadened at base. 
Surface between setae sharply microscopically granulose 
on spire (smoother on body whorl) and finely radially 
wrinkled. Periphery broadly rounded. Base tumid, papil- 
lose where setae worn off; setae shorter than on spire, 
extending into umbilicus. Umbilicus contained about 14 
times in diameter. Body whorl weakly to moderately de- 
flected downward, constricted behind lip. Aperture broadly 
auriculate; peristome shallowly concave in profile, at angle 
of about 35° to shell axis. Lip turned outward and reflected, 
especially at base; basal lip sometimes with faint, elongate 
internal thickening. Parietal lamella usually absent (but 
present in the holotype and in San Francisco Presidio 
population). Inner part of basal lip straight or gently curved 


forward, moderately dilated, covering about half of um- 
bilicus. Periostracum warm brown; lip pinkish buff. 


Description of soft anatomy: Eight specimens from San 
Bruno Mountain (regarded as virtual topotypes for the 
reasons discussed below) were dissected. 

Color of living animals tan to brown, darker and grayer 
on body-stalk. Mantle over lung 10-50% maculated with 
black. 

Atrium (Figure 4) of moderate length for genus. Penis 
elongate-conical, with anterior, basal portion enclosed in 
thin sheath adnate to base. Penial retractor muscle inserted 
on epiphallus. Retentor muscle extending from penial re- 
tractor muscle at attachment on epiphallus to summit of 
penial sheath, from which other thin retentor fibers form 
connections with parts of epiphallus and vas deferens. In- 
terior of penial chamber bearing papillose pilasters in di- 
verging V-pattern (Figure 5). Slender peduncular section 
of about 2.0 mm present between base of sheath and junc- 
tion with atrium. 

Sheathed part of penis in specimen shown in Figure 4 
about 5.0 mm in length, protruding part about 3.5 mm. 
In other specimens from same locality, sheathed part vary- 
ing from 4.0 to 5.4 mm (mean 4.5 mm); protruding part 
varying from 3.4 to 4.6 mm (mean 3.9 mm). Mean ratio 
of protruding length to sheathed length about 0.87. 

Apex of penis containing short, conical, pointed verge 
0.5 mm long and 0.3 mm wide at base. Seminal duct 
opening into penial chamber at tip of verge; tip of verge 
split into two opposing lips about 0.1 mm long (Figure 6). 

Spermathecal duct relatively small and narrow, tightly 
appressed to free oviduct (which is smaller in diameter 
and branches from it), cylindrical-conic, about 2.5 mm 
long, about 1.0 mm in diameter at junction with oviduct, 
tapering gradually to 0.4 mm constriction at base of sper- 
matheca. 

Spermatheca elongate-ovate, rather slender in fully ma- 
ture specimens, narrowly cylindrical in less mature indi- 
viduals, about 3.5 mm long, with rounded tip. 


Type material: Holotype: ANSP 11142a (BAKER, 1962). 
Paratype: UCM 16202 (Wu & BRANDAUER, 1982). 


B. Roth & W. B. Miller, 1993 


Explanation of Figures 4 to 6 


Figures 4-6. Vespericola pilosus (Henderson). Drawings made 
from projections of stained whole mounts. Figure 4. Anterior 
portion of reproductive system, SBMNH 36089, CALIFORNIA: 
San Mateo County: N slope of San Bruno Mountain facing 
Guadalupe Canyon, W. B. Miller coll., 24 August 1991. Figure 
5. Penis with protruding portion opened to show verge and pa- 


Page 137 


Distribution: CALIFORNIA: San Francisco City and Coun- 
ty (ANSP, SBMNH, UCM): Presidio (CAS); Lobos Creek 
(CAS); near Mountain Lake (CAS); Golden Gate Park 
(CAS); Lake Merced (CAS). San Mateo County: N slope 
of San Bruno Mountain facing Guadalupe Canyon (BR, 
SBMNH); Colma (BR, CAS); Half Moon Bay (SBMNH); 
canyon back of Half Moon Bay (CAS); Pilarcitos Creek 
(CAS); Purisima Creek Canyon near mouth of Walker 
Gulch (BR); San Gregorio (CAS). 


Remarks: The type locality of Vespericola pilosus is San 
Francisco, with no more exact location specified. The spe- 
cies is not known to have been collected within the city 
limits of San Francisco in recent years; we have searched 
the San Francisco localities cited above, and others, without 
finding it. Given the extent of habitat modification in the 
urban environment, it is unlikely that the type population 
is still extant. However, the species is moderately common 
on San Bruno Mountain in northern San Mateo County, 
Just across the county line from San Francisco. The coastal 
brushfield and chaparral vegetation there was at one time 
continuous with that of the San Miguel Hills of south- 
central San Francisco. We have therefore based our shell 
and anatomical observations on samples from San Bruno 
Mountain and consider them to represent typical V. pilosus. 

Previous authors used the name Vespericola (or Poly- 
gyra) columbiana pilosa to refer to samples with setose 
periostracum, whatever their provenance. The name was 
not applied in the sense of a geographically delimited sub- 
species. HENDERSON (1928:143) stated, “this race ranges 
from Alaska to San Francisco Co., Cal.” A periostracum 
with setae occurs in specimens from Alaska to central 
California and is, in fact, the predominant condition 
throughout the range of V. columbianus. Topotypic and 
near-topotypic specimens of V. columbianus collected by 
the junior author are setose. We have not yet located any 
populations characterized by absence of setae, and consider 
the taxonomic significance of this character to be undemon- 
strated. 

However, specimens from San Francisco and vicinity 
differ in reproductive system anatomy and details of shell 
shape from samples from farther north. Populations from 
the San Francisco peninsula (which include the type pop- 
ulation of Polygyra columbiana pilosa Henderson) are here 
assigned to Vespericola pilosus, which is separated as a 
distinct species; populations from Marin County are de- 
scribed as a new species, V. marinensis. We provisionally 


_— 


pillose pilasters, SBMNH 36090, collection data same as above. 
Figure 6. Verge and part of epiphallus, showing seminal duct in 
dashed lines with opening between apical lips, SBMNH 36091, 
collection data same as above. Abbreviations for anatomical fig- 
ures: at, atrium; cp, cut edge of penis; ep, epiphallus; go, genital 
orifice; ov, oviduct; pe, penis; pi, pilaster; pr, penial retractor; 
ps, penial sheath; pt, prostate; re, retentor; sc, cavity of penial 
sheath; sd, spermathecal duct; sp, spermatheca; ut, uterus; va, 
vagina; vd, vas deferens; ve, verge. Scale lines in anatomical 
figures = 1 mm. 


Page 138 


The Veliger, Vol. 36, No. 2 


Explanation of Figures 7 to 10 


Figures 7-10. Vespericola columbianus (Lea). Figure 7. Shell, SBMNH 36092, WasHINGTON: Clark County: 
Ridgefield Wildlife Refuge, near Vancouver, under log along trail, W. B. Miller coll., 21 July 1989. Diameter 
12.1 mm. Figures 8-10. Shell, SBMNH 36093, WASHINGTON: Pacific County: right bank of Columbia River 0.4 
km W of highway bridge to Astoria, Oregon, W. B. Miller coll., 12 July 1989. Top, apertural, and basal views. 


Diameter 14.0 mm. 


refer records from northwestern California and the Pacific 
Northwest to V. columbianus, sensu lato, pending a more 
comprehensive study of the anatomy of samples from 
throughout its range. 

An attempt was made to collect topotypes of Vespericola 
columbianus at Vancouver, Washington. Although the area 
has been extensively urbanized, one specimen was collected 
at the Ridgefield Wildlife Refuge north of the city (Figure 
7). Upon dissection, its anatomy was found to be too im- 
mature for comparative measurements. The following an- 
atomical notes are based on mature specimens collected 
about 130 km downstream along the right (north) bank 
of the Columbia River just west of the highway bridge to 
Astoria, Oregon (Figures 8-10). 

Color of living animals tan, darker and grayer on body- 
stalk. Mantle over lung clear buff, about 20% maculated 
with black. 

Atrium (Figure 11) of moderate length for genus. Penis 
elongate-conical, largely enclosed in thin sheath adnate to 
base. Penial retractor muscle inserted on epiphallus. Nar- 
row retentor muscle extending from penial retractor mus- 
cle at attachment on epiphallus to summit of penial sheath, 
from which other thin retentor fibers form connections with 
parts of epiphallus and vas deferens. Interior of penial 
chamber bearing papillose pilasters in diverging V-pattern 
(Figure 12). Broad peduncular section of about 1.0 mm 
present between base of sheath and junction with atrium. 

Sheathed part of penis about 5.0 mm in length; pro- 
truding part about 0.2 mm. Apex of the penis containing 
short, conical, pointed verge 1.0 mm long and 0.5 mm wide 
at base. Seminal duct opening into penial chamber at tip 
of verge through minute slit (Figure 13). 

Spermathecal duct short and massive, appressed to free 
oviduct (which is smaller in diameter and branches from 
it), cylindrical-conic, about 2.0 mm long, about 1.5 mm in 
diameter at junction with oviduct, tapering sharply to 0.5 
mm constriction at base of spermatheca. 

Spermatheca oblong-ovate in fully mature specimens, 
narrowly cylindrical in less mature individuals, about 4.0 
mm long, with rounded tip. 


Numerous additional specimens of Vespericola colum- 
bianus were examined, ranging from Prince Rupert and 
the Queen Charlotte Islands, British Columbia, to the 
valley of the Columbia River, Washington-Oregon. A con- 
sideration of the variation within the species over its range 
is beyond the scope of this paper. However, a summary 
of characters based on 69 dissected specimens is as follows: 
mantle over the lung 10-90% maculated with black; 
sheathed part of penis 3.6-8.5 mm long (mean 5.7 mm); 
protruding part of penis 0-1.4 mm long (mean 0.6 mm). 
(In seven specimens from three localities in British Co- 
lumbia [Bridal Veil Falls, Hope District; Port Hardy, 
Vancouver Island; and Graham Island, Queen Charlotte 
Islands], penial sheath extending 0.5-4.2 mm above sum- 
mit of penis.) Verge 0.8-2.0 mm long; spermathecal duct 
1.5-3.0 mm long. 

The main anatomical characters that distinguish Ves- 
pericola columbianus are its stout penial complex, with the 
sheath completely or almost completely enveloping the pe- 
nis in mature specimens, and the moderately long, conical, 
pointed verge at the apex of the penial chamber. The 
spermathecal duct is short and thick at its junction with 
the oviduct. 

Vespericola pilosus differs anatomically from V. colum- 
bianus by the long protruding portion of its penis, its much 
shorter verge, and its narrower, more slender spermathecal 
duct and spermatheca. It is distinguished from V. mari- 
nensis, next described, by having the sheathed length of 
the penis equal to or greater than the protruding length, 
a verge half or less the length of the verge of V. marinensis, 
and a more slender spermathecal duct. Table 1 summarizes 
the major differences among these taxa. 

The periphery of the shell of Vespericola pilosus is broad- 
ly rounded; that of V. columbianus is usually weakly suban- 
gulate to at least the last 0.5 whorl. The periostracal setae 
of V. pilosus tend to be denser (19-30/mm/7) than those of 
V. columbianus (7-19/mm/? in the specimens examined) 
and much denser than in V. marinensis (7-10/mm/?). 
Pitssry (1940) considered the typical form of V. colum- 
bianus generally to lack setae, but all specimens we have 


B. Roth & W. B. Miller, 1993 


= igre =D 
TT ee ee eT BO 


JZ 


Us 


Page 139 


seen have (or originally had) setae, although they have 
been rubbed off some museum specimens. 

The habitat of Vespericola pilosus includes moist spots 
in coastal brushfield and chaparral vegetation; under leaves 
of cow-parsnip (Heracleum lanatum); around spring seeps; 
in leafmold along streams; and in alder woods. 

The earlier citation of the taxon as “Vespericola pilosa’ 
by BAKER (1962) was not a taxonomic revision but merely 
a convention of that publication, a list of type material in 
the ANSP. 

For purposes of the American Fisheries Society list of 
the common names of mollusks (TURGEON et al., 1988) 
and other administrative uses, we propose the name 
“brushfield hesperian.” 


> 


Vespericola marinensis Roth & Miller, sp. nov. 
(Figures 14-19) 


Vespericola columbiana pilosa (Henderson): PILsBRy, 1940: 
896-898 (in part; records from Marin County, Cali- 
fornia, only); INGRAM, 1946:92 (in part); INGRAM & 
Lotz, 1950:25-26 (in part). Non Vespericola pilosus 
(Henderson, 1928). 


Diagnosis: A small to medium-sized Vespericola with de- 
pressed-helicoid to broadly conical, narrowly umbilicate 
shell, 5.4-5.9 whorls, 7-10 periostracal setae/mm?, and 
no parietal lamella. Penis elongate-conical, ratio of pro- 
truding part to sheathed part approximately 1.6; verge 
0.7-1.8 mm long, conical, ending in 0.1 mm opposing lips. 


Description of shell: Shell small to medium-sized for the 
genus (diameter 10.5-15.0 mm) depressed-helicoid to 
broadly conical, narrowly umbilicate, with 5.4—5.9 whorls. 
Spire straight-sided or very weakly convex; whorls round- 
ed, suture moderately to strongly impressed. Embryonic 
whorls 1.5-1.8, with prominent, sharp to rounded, radial 
wrinkles surmounted by smooth, hemispheric to radially 
elongate papillae. Early teleoconch whorls with incon- 
spicuous, crowded, retractive growth rugae and close-set, 
regular granulation with collabral trend. Periostracum 
bearing slender setae in diagonal, often steeply descending, 
rows; setae 7-10/mm/’, approximately 0.3-0.35 mm long 


Explanation of Figures 11 to 13 


Figures 11-13. Vespericola columbianus (Lea). Drawings made 
from projections of stained whole mounts. Figure 11. Anterior 
portion of reproductive system, SBMNH 36094, WASHINGTON: 
Pacific County: right bank of Columbia River just W of highway 
bridge to Astoria, Oregon, W. B. Miller coll., 12 July 1989. 
Figure 12. Penis with protruding portion opened to show verge 
and papillose pilasters, SBMNH 36095, BRITISH COLUMBIA: 
Naikoon Provincial Park, Graham Island, Queen Charlotte Is- 
lands, W. B. Miller and E. S. Miller coll., 22-24 June 1991. 
Specimen slightly immature as indicated by small spermatheca 
and penial sheath not enveloping entire penis. Figure 13. Verge 
and part of epiphallus, showing seminal duct in dashed lines with 
opening in apical slit, SBMNH 36096, collection data same as 
for preceding specimen. 


Page 140 


The Veliger, Vol. 36, No. 2 


Explanation of Figures 14 to 16 


Figures 14-16. Vespericola marinensis Roth & Miller, sp. nov. Shell, holotype, SBMNH 36080, CALIFORNIA: 
Marin County: Bear Valley Trail, Point Reyes, W. B. Miller coll., 23 April 1990. Top, apertural, and basal views. 


Diameter 12.2 mm. 


on spire and shoulder of body whorl, erect or curving away 
from direction of coiling, sometimes with recurved tip, 
moderately broadened at base. Surface between setae 
densely, smoothly granulose on spire and body whorl and 
collabrally wrinkled. Periphery simply rounded, not sub- 
angulate. Base tumid, densely papillose; with setae ex- 
tending into umbilicus. Umbilicus contained about 13-16 
times in diameter. Body whorl deflected downward except 
immediately behind aperture, sharply constricted behind 
lip. Aperture broadly auriculate; peristome shallowly con- 
cave in profile, at angle of 25° to 45° to shell axis. Lip 
turned outward and expanded, somewhat reflected at base; 
basal and outer lips sometimes thickened submarginally. 
Parietal lamella absent. Inner part of basal lip gently an- 
gled forward, weakly to moderately dilated, covering 4 to 
4 of umbilicus. Periostracum warm brown; lip pale tan 
to white. 


Dimensions of holotype: Diameter (exclusive of expand- 
ed lip) 12.2 mm, height 8.7 mm, whorls 5.6. 


Description of soft anatomy: The holotype and 66 ad- 
ditional specimens were dissected. 

Color of living animals tan to brown on foot, darker 
and grayer on body-stalk. Mantle over lung 15-30% mac- 
ulated with black. 

Atrium (Figure 17) of moderate length for genus. Penis 
elongate-conical, anterior, basal portion enclosed in thin 
sheath adnate to base. Penial retractor muscle inserted on 
epiphallus. Narrow retentor muscle extending from penial 
retractor muscle at attachment on epiphallus to summit of 
penial sheath, from which other thin retentor fibers form 
connections with parts of epiphallus and vas deferens. In- 
terior of the penial chamber bearing papillose pilasters in 
diverging V-pattern (Figure 18). Short, broad peduncular 
section of about 0.8 mm present between base of sheath 
and junction with atrium. 

Sheathed part of penis in specimen shown in Figure 17 
about 4.8 mm in length, protruding part about 8.8 mm. 
In remaining specimens, sheathed part varying from 3.4 


Table 1 


Summary of dimensions (in mm), ratios, and selected characters in Vespericola columbianus, V. pilosus, V. marinensis, 
and V. orius. Statistics are range with mean in parentheses. Only adult specimens included. 


Character 7, columbianus V. pilosus 
Mantle over lung, coverage by 10-90% 10-50% 
dark maculation 
Sheathed part of penis 3.6-8.5 (5.7) 4.0-5.4 (4.5) 
Protruding part of penis 0.0-1.4 (0.6) 3.4-4.6 (3.9) 


Ratio of protruding part to 
sheathed part 


Verge, length 
Verge, end 


mean *0.11 


0.8-2.0 (1.2) 


minute slit 


mean ~0.87 


0.5-0.6 (0.5) 


apical slit forming 0.1 
mm lips 


Spermathecal duct 1.5-3.0 (2.6), 2.5, slender 
massive 

Spermatheca, length 4.0 3.5 

Peduncular section of penis 1.0 2.0 

Periphery weakly subangu- broadly rounded 
late 

Periostracal setae/mm7? 7-19 19-30 


V. marinensis 


15-30% 


3.4-6.0 (4.4) 
4.8-10.8 (7.0) 
mean ~1.6 


0.7-1.8 (1.1) 


apical slit forming 0.1 
mm lips 
=3.0, massive 


3.2 
0.8 
broadly rounded 


7-10 


V. orws 


30-40% 


2.5-3.0 (2.7) 


0.15-0.20 (0.18) 
conical 


=2.0, slender 


=2.7 
1.0 


usually weakly sub- 
angulate 


11-17 


B. Roth & W. B. Miller, 1993 


19 


Page 141 


to 6.0 mm (mean 4.4 mm); protruding part varying from 
4.8 to 10.8 mm (mean 7.0 mm). Mean ratio of protruding 
length to sheathed length about 1.6. 

Apex of penis containing short, conical, pointed verge 
varying from 0.7 to 1.8 mm long, 0.3 mm wide at base. 
Seminal duct opening into penial chamber at tip of verge 
through apical slit which forms two opposing lips about 
0.1 mm long (Figure 19). 

Spermathecal duct massive, tightly appressed to free 
oviduct (which is smaller in diameter and branches from 
it), cylindrical-conic, about 3.0 mm long, about 1.3 mm in 
diameter at junction with oviduct, tapering gradually to 
0.4 mm constriction at base of spermatheca. 

Spermatheca oblong-ovate in fully mature specimens, 
narrowly cylindrical in less mature individuals, about 3.2 
mm long, with rounded tip. 


Type material: Holotype: SBMNH 36080 (shell and dis- 
sected anatomy), CALIFORNIA: Marin County: Bear Valley 
Trail, Point Reyes, W. B. Miller coll., 23 April 1990. 

Paratypes: SBMNH 36081 (4 shells and stained whole 
mount of reproductive system), from same locality as ho- 
lotype. Additional paratypes (all, CALIFORNIA: Marin 
County:), SBMNH 36082 (4), along Bear Valley Trail 
ca. 2.0 km inland from Arch Rock, under logs and bark, 
W. B. Miller coll., 1 January 1989. SBMNH 36083 (1), 
along Bear Valley Trail, ca. 0.8 km from Arch Rock, W. 
B. Miller coll., 25 July 1989. SBMNH 36084 (1), along 
Bear Valley Trail, ca. 0.8 km from Arch Rock, under log, 
W. B. Miller coll., 20 September 1990. SBMNH 36085 
(2), Bear Valley Trail, W. B. Miller and E. S. Miller 
coll., 24-29 April 1988. SBMNH 36086 (7), Bear Valley 
Trail, between Wilderness boundary and Arch Rock, un- 
der logs along trail, W. B. Miller coll., 13 November 1989. 
Paratypes also deposited in ANSP, CAS, LACM, and 
USNM. 


Referred material: CALIFORNIA: Marin County: Dillon 
Beach (CAS); Tomales Point (CAS); head of first large 
east-draining draw N of Whites Gulch (BR, SBMNH), 
McClures Beach parking area (BR), side canyon of Home 
Ranch Creek Canyon (BR), Muddy Hollow Trail 
(SBMNH); Kehoe Beach (BR, SBMNH) (all, Point Reyes 
Peninsula); Inverness (BR, SBMNH); Point Reyes Sta- 
tion (CAS); Olema Creek (BR); 1.6 km SW of California 
Hwy. 1 bridge over Walker Creek, E side of Tomales Bay 


Explanation of Figures 17 to 19 


Figures 17-19. Vespericola marinensis Roth & Miller, sp. nov. 
Drawings made from projections of stained whole mounts. Figure 
17. Anterior portion of reproductive system of holotype, SBMNH 
36080, CALIFORNIA: Marin County: Bear Valley Trail, Point 
Reyes, W. B. Miller coll., 23 April 1990. Figure 18. Penis with 
protruding portion opened to show verge and papillose pilasters, 
SBMNH 36087, CaALirornia: Marin County: Muddy Hollow 
Trail, Point Reyes, W. B. Miller coll., 20 April 1990. Figure 
19. Verge, SBMNH 36088, Cauirornia: Marin County, Alpine 
Dam, W. B. Miller and B. Roth coll., 16 January 1991. 


Page 142 


The Veliger, Vol. 36, No. 2 


Explanation of Figures 20 to 22 


Figures 20-22. Vespericola orius (Berry). Shell, BR 330, CALIFORNIA: El Dorado County: Eagle King Mine, Grizzly 
Flats, E. P. Chace and E. M. Chace coll., autumn 1938. Top, apertural, and basal views. Diameter 13.0 mm. 


(BR); Walker Creek, 0.4 km above mouth of Chileno 
Creek (BR); Taylorville (SBMNH); San Geronimo Creek 
near Forest Knolls (BR); Mesa Road, ca. 3 km NW of 
Bolinas (BR, SBMNH); debris above high tide line, N 
end of Bolinas Lagoon (BR) Lagunitas Creek, 0.3 km 
below Alpine Dam (BR, SBMNH); Alpine Dam 
(SBMNH); near Stinson Beach (CAS); near Fairfax 
(CAS); Ross (SBMNH); San Rafael (CAS); Muir Woods 
(CAS); Sausalito (SBMNH); Point Bonita (CAS). 


Remarks: In the type material, adult shell diameter ranges 
from 11.6 to 14.0 mm (mean of 24 specimens including 
holotype, 12.57 mm); height, 8.0 to 9.5 mm (x = 8.65 
mm); height-diameter ratio, 0.63 to 0.73 (x = 0.689); 
number of whorls, 5.4 to 5.9 (x = 5.68). The largest shells 
examined are from Walker Creek, 0.4 km above mouth 
of Chileno Creek, reaching 15.0 mm in diameter and 9.6 
mm in height. Small shells, adult at 10.5 mm diameter, 
occur on the northern part of the Point Reyes Peninsula, 
as at Tomales Point and near Whites Gulch. 

The shell of Vespericola marinensis differs from that of 
V. pilosus and V. orius in having fewer setae per millimeter 
and in having the surface between the setae densely covered 
by smooth, round to radially elongated granules. In V. 
pilosus the granulation is sharper on the spire, usually 
becoming weak or obsolete on the body whorl. In V. orius 
granulation is weak throughout. 

Vespericola marinensis is distinguished anatomically 
from other species by its moderately long, pointed verge, 
with apical slit forming two opposing lips, in a narrowly 
elongated penis protruding for more than half of its length 
from the basal penial sheath. It differs from V. pilosus by 
its longer verge (more than twice the length of the V. pilosus 
verge) and by its longer protruding part of the penis. It 
differs from V. columbianus by the much longer protruding 
part of the penis, which is never completely enclosed by 
the penial sheath. 

The habitat includes moist spots in coastal brushfield 
and chaparral vegetation; under leaves of cow-parsnip 
(Heracleum lanatum); around spring seeps; in leafmold 
along streams; in alder woods; and in mixed evergreen 
forest. 


INGRAM & Lotz (1950) reported Vespericola columbiana 
pilosa from Hacienda, Sonoma County. PILsBRy (1928) 
reported it (as Polygyra) from Russian River, presumably 
in Sonoma, rather than Mendocino, County. We have not 
examined specimens from these localities, and do not know 
whether they represent northern records of V. marinensis. 
The occurrences are within the range of Vespericola me- 
gasoma (Pilsbry, 1928). 

For purposes of the American Fisheries Society list of 
the common names of mollusks (TURGEON et al., 1988) 
and other administrative uses, we propose the name ‘“‘Ma- 
rin hesperian.” 


Etymology: The species is named for Marin County. 


Vespericola orius (Berry, 1933) 
(Figures 20-24) 


Polygyra columbiana oria BERRY, 1933:15, pl. 2, figs. 11, 11a. 
Vespericola columbiana oria (Berry): PILSBRY, 1940:900-901, 
fig. 516; INGRAM, 1946:92. 


Diagnosis: A medium-sized Vespericola with depressed- 
helicoid to broadly conical, umbilicate shell, 5.2-6.25 
whorls, 11-17 periostracal setae/mm?’, and no parietal 
lamella. Penis short, stout, completely enclosed in sheath, 
apical portion slender and tubular, containing 0.15-0.20 
mm long, conical verge. 


Description of shell: Shell thin, medium-sized for the 
genus (diameter 11.6-16.4 mm) depressed-helicoid to 
broadly conical, umbilicate, with 5.2-6.25 whorls. Spire 
straight-sided or very weakly convex; whorls rounded, su- 
ture moderately impressed. Embryonic whorls 1.5-1.8, 
most often with prominent, sharp, radial wrinkles sur- 
mounted by smooth, round to radially elongate papillae, 
but wrinkles sometimes faint and surface between papillae 
smooth. Early teleoconch whorls with inconspicuous, 
crowded, retractive growth rugae, very slightly granular. 
Periostracum bearing slender setae in gently descending 
rows; setae 11-17/mm/’, approximately 0.3 mm long on 
spire and shoulder of body whorl, erect or curving away 


B. Roth & W. B. Miller, 1993 


from direction of coiling, not greatly broadened at base but 
sometimes with triangular basal lamina abaperturally. 
Surface between setae finely radially wrinkled, locally with 
patches of minute granulation. Periphery usually with a 
trace of angulation, at least before last 0.5 whorl; some- 
times simply rounded. Base tumid, with setae shorter than 
on spire, extending into umbilicus. Umbilicus contained 
11-14 times in diameter. Body whorl weakly to moderately 
deflected downward, constricted behind lip. Aperture 
broadly auriculate; peristome shallowly concave in profile, 
at angle of about 35° to shell axis. Lip turned outward 
and reflected, especially at base; not conspicuously thick- 
ened. Parietal lamella absent. Inner part of basal lip curved 
or angled forward, moderately dilated, covering 4 to 4 
(usually % or less) of umbilicus. Periostracum warm brown; 
lip pinkish buff. 


Description of soft anatomy: Twelve specimens were 
dissected. 

Color of living animals tan, darker and grayer on body- 
stalk. Mantle over lung clear buff, 30-40% maculated with 
black. 

Atrium (Figure 23) of moderate length for genus. Penis 
short and stout, completely enclosed in thin sheath adnate 
to base. Apical part of penis slender and tubular, of same 
diameter as epiphallus, containing minuscule verge. Sheath 
extending above summit of penis, enclosing portion of epi- 
phallus. Penial retractor muscle inserted on epiphallus. 
Narrow retentor muscle extending from penial retractor 
muscle at attachment on epiphallus to summit of penial 
sheath, from which other thin retentor fibers form con- 
nections with parts of epiphallus and vas deferens. Short 
peduncular section of about 1.0 mm present between base 
of sheath and junction with atrium. 

Length of penis, from base to verge, in figured specimen 
about 2.5 mm; sheathed part of epiphallus about 1.3 mm; 
total sheath length 3.8 mm. In other specimens, length of 
penis varying from 2.5 to 3.0 mm (mean 2.7 mm; total 
length of the sheath varying from 3.4 to 4.2 mm (mean 
3.9 mm). 

Verge within narrow, tubular, apical portion of the 
penis, about 0.15 to 0.20 mm long, 0.20 mm wide at base 
(Figure 24). Seminal duct opening into penis through tip 
of verge. 

Spermathecal duct small and narrow, tightly appressed 
to free oviduct, which is of equal diameter and branches 
from it, cylindrical-conic, about 2.0 mm long, about 0.7 
mm in diameter at junction with oviduct, tapering grad- 
ually to 0.3 mm constriction at base of spermatheca. 

Spermatheca oblong-ovate in fully mature specimens, 
narrowly cylindrical in less mature individuals, about 2.7 
mm long, with rounded tip. 


Type material: Holotype: SBMNH 34203, CALIFORNIA: 
El Dorado County: canyon of South Fork of American 
River near Riverton. 

Paratypes: CAS 064120, CAS 066614, SBMNH 34204, 
from same locality as holotype. 


Imm 


Explanation of Figures 23 and 24 


Figures 23, 24. Vespericola orius (Berry). Drawings made from 
projections of stained whole mounts. Figure 23. Anterior portion 
of reproductive system, SBMNH 36097, Catirornia: El Dorado 
County: along left bank of North Fork of Cosumnes River at 
crossing of Cosumnes Mine Road, W. B. Miller coll., 21 January 
1991. Figure 24. Enlarged section of epiphallus and apical por- 
tion of penis to show location of verge, SBMNH 36098, collection 
data same as above. 


Distribution: CALIFORNIA: El Dorado County: Placerville 
(CAS); near Camp Creek, 4.8 km E of Pleasant Valley 
(CAS); along left bank of North Fork of Cosumnes River 
at crossing of Cosumnes Mine Road, W. B. Miller coll., 
21 January 1991 (SBMNH); Eagle King Mine, near 
Grizzly Flat (CAS, BR); South Fork of American River 
near Riverton (CAS). 


Remarks: The epiphallus and the apical part of the penis 
form a continuous tube of constant diameter, with no ex- 
ternal differentiation. There is no bulge or swelling at the 
level of the verge. Only at about 0.5 mm below the verge 
does the penis enlarge abruptly into a capacious cavity. 


Page 144 


This gives the appearance that the verge is located well 
up in the epiphallus; but, by convention, the portion of the 
male sperm-delivering duct below the base of the verge 
and above the atrium, everted in copulation, is defined as 
the penis. It seems probable to us that the slender part of 
the duct below the base of the verge is homologous with 
the summit of the penial sac in other species of Vespericola. 

Vespericola orius is distinguished anatomically from oth- 
er species by its minuscule verge located in a narrow, 
tubular, prolongation of the apex of the penial chamber; 
by its short, stout penis in a penial sheath overlapping a 
sizeable part of the epiphallus; and by its small, narrow 
spermathecal duct. 

The inner end of the basal lip of the aperture is more 
distinctly angled forward than in Vespericola pilosus and 
covers, on the average, less of the umbilicus. The surface 
between the periostracal setae is less granulose than in V. 
pilosus, especially on the spire. 

For purposes of the American Fisheries Society list of 
the common names of mollusks (TURGEON et al., 1988) 
and other administrative uses, we propose the name “El 
Dorado hesperian.”’ 


OTHER RECORDS OF 
Vespericola columbianus IN 
CALIFORNIA 


In museum collections, shells in which the inner lip is not 
markedly dilated over the umbilicus are often identified as 
Vespericola columbianus. On the basis of our previous find- 
ings, we believe such identifications require confirmation 
by dissection. 

PILsBRY (1940) reported Vespericola columbianus pilosus 
from Crescent City, Del Norte County, and San Pablo, 
Contra Costa County, California. Our collecting along the 
coast of Del Norte County has not turned up any V. 
columbianus, but rather Vespericola megasoma, Vespericola 
euthales (Berry, 1939), and two new species, outwardly 
similar to V. megasoma, that will be described and discussed 
in a future paper. 

Museum collections contain samples resembling Ves- 
pericola pilosus from several localities in Contra Costa and 
Alameda counties. The shells are, in general, more de- 
pressed and more widely umbilicate than those of V. pilosus 
from the San Francisco Peninsula, with the inner part of 
the basal lip angled rather sharply forward. A parietal 
lamella is absent. We are in the process of trying to locate 
living populations for anatomical data. 


LITERATURE CITED 


BAKER, H.B. 1962. Type land snails in the Academy of Natural 
Sciences of Philadelphia. I. North America, north of Mexico. 
Proceedings of the Academy of Natural Sciences of Phila- 
delphia 114(1):1-21. 

Berry, S.S. 1933. Three new polygyrid snails from California. 
Nautilus 47(1):12-16, pl. 2. 

EMBERTON, K. C. 1988. The genitalic, allozymic, and concho- 


The Veliger, Vol. 36, No. 2 


logical evolution of the eastern North American Triodop- 
sinae (Gastropoda: Pulmonata: Polygyridae). Malacologia 
28(1-2):159-273. 

EMBERTON, K. C. 1989. POLYGYRIDAE Pilsbry, 1894 (Mol- 
lusca, Gastropoda): proposed precedence over MESODONTI- 
DAE Tryon, 1866. Bulletin of Zoological Nomenclature 46(2): 
94-96. 

EYERDAM, W. J. 1951. A collection of mollusks from Wash- 
ington Bay, Kuiu Island, southeastern Alaska. Minutes of 
the Conchological Club of Southern California, No. 114:7- 
ible 

HENDERSON, J. 1928. Polygyra columbiana pilosa, new subspe- 
cies. Nautilus 41(4):143. 

HENDERSON, J. 1929. The non-marine Mollusca of Oregon 
and Washington. University of Colorado Studies 17(2):47- 
190. 

HENDERSON, J. 1936. The non-marine Mollusca of Oregon 
and Washington—Supplement. University of Colorado 
Studies 23(4):251-280. 

ICZN (INTERNATIONAL COMMISSION ON ZOOLOGICAL NOMEN- 
CLATURE). 1992. OPINION 1691. Polygyra Say, 1818 (Mol- 
lusca, Gastropoda): Polygyra septemvolva Say, 1818, desig- 
nated as the type species, and POLYGYRIDAE Pilsbry, 
1895 given precedence over MESODONTIDAE Tryon, 
1866. Bulletin of Zoological Nomenclature 49(3):240-241. 

INGRAM, W. M. 1946. A check list of the helicoid snails of 
California from Henry A. Pilsbry’s monograph. Bulletin of 
the Southern California Academy of Sciences 45(2):61-93. 

INGRAM, W. M. & C. Lorz. 1950. Land mollusks of the San 
Francisco Bay counties. Journal of Entomology and Zoology 
42(1):5-27. 

La Rocqug, A. 1953. Catalogue of the Recent Mollusca of 
Canada. National Museum of Canada Bulletin, No. 129, 
Biological Series, No. 44:i-1x, 1-406. 

MILLER, W.B. 1967. Anatomical revision of the genus Sonorella 
(Pulmonata: Helminthoglyptidae). Unpublished Ph.D. Dis- 
sertation, Department of Biological Sciences, University of 
Arizona. xiil + 293 pp. 

PiusBry, H. A. 1928. Species of Polygyra from Montana, Idaho, 
and the Pacific coast states. Proceedings of the Academy of 
Natural Sciences of Philadelphia 80:177-186. 

PiussBry, H. A. 1939. Land Mollusca of North America (north 
of Mexico). Academy of Natural Sciences of Philadelphia 
Monograph 3, 1(1):i-xvii, 1-573, i-1x. 

PiusBry, H. A. 1940. Land Mollusca of North America (north 
of Mexico). Academy of Natural Sciences of Philadelphia 
Monograph 3, 1(2):i-vii, 574-994, i-ix. 

Rotu, B. 1985. A new species of Vespericola (Gastropoda: 
Pulmonata: Polygyridae) from the Klamath Mountains, 
California. Wasmann Journal of Biology 42(1/2):84-91. 

TurGEoN, D. D., A. E. BoGan, E. V. Coan, W. K. EMERSON, 
W.G. Lyons, W. L. PRaTT, C. F. E. ROPER, A. SCHELTEMA, 
F. G. THOMPSON & J. D. WILLIAMS. 1988. Common and 
scientific names of aquatic invertebrates from the United 
States and Canada: mollusks. American Fisheries Society 
Special Publication 16. viii + 277 pp., 12 pls. 

Wess, G. R. 1970. Observations on the sexology of Vespericola 
columbiana (Lea) from Olympic Peninsula, Washington. 
Gastropodia 1(8):75-77. 

Wu, S.-K. & N. E. BRANDAUER. 1982. Type specimens of 
Recent Mollusca in the University of Colorado Museum. 
University of Colorado Museum Natural History Inventory 
of Colorado, No. 7:1-47. 

ZILCH, A. 1959-1960. Gastropoda, Teil 2, Euthyneura. Hand- 
buch der Paldozoologie 6(2):1-400 (1959); 401-834 (1960). 


The Veliger 36(2):145-159 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Slugs of Portugal. HI. Revision of the Genus 
Geomalacus Allman, 1843 


(Gastropoda: Pulmonata: Arionidae) 


T. RODRIGUEZ, P. ONDINA, A. OUTEIRO, anp J. CASTILLEJO 


Departamento de Bioloxia Animal, Facultade de Bioloxia, Universidade de Santiago de Compostela, 
15706 Santiago de Compostela, La Coruna, Spain 


Abstract. This study revises the genus Geomalacus in Portugal and compares specimens found there 
with those found in Ireland, where it is represented by Geomalacus maculosus, and specimens encountered 
in Spain. The anatomy of the specimens is also described with the belief that they all belong to three 
species: Geomalacus maculosus, G. oliveirae, and G. anguiformis. 


INTRODUCTION 


The genus Geomalacus (type species G. maculosus) was 
created by ALLMAN in 1843 to include certain long-bodied 
slugs with large palish marks, pneumostome on the lower 
third of the shield, genital orifice between the shield and 
the lower right tentacle, very small caudal mucus pore, 
and quite solid, flat limacella (GERMAIN, 1930). The sem- 
inal receptacle of species in this genus does not open di- 
rectly into the atrium; rather it does so in a large (in most 
cases) vaginal diverticulum. 

POLLONERA (1890) considered the subgenus Geomalacus 
as typical of pale-spotted slugs, with the sexual organs 
arranged differently from striped species. He formed the 
subgenus Arrudia for species of Geomalacus that have dark 
lateral bands instead of spots on the back, and whose 
genital apparatus resembles that of Arion. Arrudia is dis- 
tinguished from Ariunculus by its smaller caudal gland, its 
reproductive apparatus, and by the presence of limacellae. 
Pollonera included Geomalacus anguiformis Morelet, 1845, 
Geomalacus squammantinus Morelet, 1845, and Geomala- 
cus oliverrae Simroth, 1891, in the subgenus Arrudia, and 
G. maculosus in the subgenus Geomalacus. 

Four species of Geomalacus have been reported or de- 
scribed in Portugal: G. (Geomalacus) maculosus Allman, 
1843, G. (Arrudia) anguiformis (Morelet, 1845), G. (Ar- 
rudia) oliveirae Simroth, 1891, G. (Geomalacus) grandis 
Simroth, 1893. 


PREVIOUS WORK IN THE 
IBERIAN PENINSULA 


Geomalacus maculosus Allman, 1843 


Geomalacus maculosus was described by ALLMAN in 1843 
from specimens collected at Carogh Lake in Country Ker- 
ry, Ireland. 

Dr. Paul Fischer reported the abundance of this species 
in Asturias (NW Spain) and in 1868 Lucas von Heyden 
found a single specimen in Santa Albas (Asturias) (in 
‘TAYLOR [1907]). SttvA & Castro (1873) had found an 
individual adult in the Monte de Sao Silvestre, near Viana 
do Castelo, which they described as Letourneuxia lusitana, 
later to be synonymized as Limax lusitanus by MORELET 
(1877). SIMROTH (1891) made observations of 40 juveniles 
collected in the Serra de Gerés in north Portugal. He 
admitted that this was not the first report of the species in 
Portugal. 

TAYLOR (1907) and HIDALGO (1916) recompiled the 
previous reports of this species in Portugal and Spain. 
Quick (1960) said this species was found in Portugal, 
Spain, Vannes (Brittany, France) and southeastern Ire- 
land. NoBRE (1941) found a single specimen close to Porto, 
and SEIXAS (1976) found several in the far north of Por- 
tugal, near the border with Galicia. 


Geomalacus grandis Simroth, 1893 


SIMROTH (1893) described a new species of the genus 
Geomalacus under the name G. grandis for specimens re- 
covered in the Serra da Estrela. NOBRE (1941) indicated 
the places where it had been found, but he did not find 
any specimens of this species. CASTILLEJO (1981b) rede- 
scribed G. grandis using material from different parts of 
Galicia (NW Spain), and CasTILLEJO & MANGA (1986) 
provided a list of the locations in Galicia and Portugal 


Page 146 


where this species appears. OUTEIRO (1988) found it at O 
Courel, Lugo (Spain). 

PLATTS & SPEIGHT (1988) thought it highly likely that 
the Portuguese material of Geomalacus grandis belonged to 
G. maculosus, as did the Spanish specimens they studied. 
Both authors went to the Serra da Estrela (Portugal) in 
October 1987 to collect material, but failed to find speci- 
mens of Geomalacus; they deduced that both species were 
possible synonyms. On the same field trip they found spec- 
imens of G. grandis at Padron (La Coruna, Spain), and 
after comparing them with their specimens of G. maculosus, 
they considered that the Galician G. grandis was the same 
as the G. maculosus of Ireland. 


Geomalacus anguiformis (Morelet, 1845), 
Limax squammantinus (Morelet, 1845), and 
Limax viridis (Morelet, 1845) 


MORELET (1845) described Limax anguiformis based on 
material collected in the Serra de Monchique (Portugal) 
and L. squammantinus and L. viridis from specimens col- 
lected in the Serra do Caldeirao (Portugal). POLLONERA 
(1890) described the internal anatomy of Geomalacus an- 
guiformis and G. squammantinus and considered G. squam- 
mantinus as a juvenile form of G. anguiformis. SIMROTH 
(1891) indicated that the form of its wrinkles on the back, 
its inability to contract greatly, the slowness of movement, 
and the fact that the head is visible only with the tentacles 
extended, put it in the genus Geomalacus. For Simroth L. 
squammantinus and L. viridis were juvenile forms of G. 
angutformis. 

SIMROTH (1893) thought that Geomalacus viridis (Mo- 
relet, 1845) was a doubtful species; he interpreted it as a 
juvenile of G. anguiformis on the basis of its appearance. 
He added that G. viridis should be rejected since its anat- 
omy was then totally unknown, making any logical as- 
signment to a species impossible. SIMROTH’s (1893) report 
was the last mention of G. anguzformis until it was collected 
by WIKTOR & PAREJO (1989) in Robeldo del Mazo (To- 
ledo, Spain), the first report of this species in Spain. 


Geomalacus oliveirae Simroth, 1891 


SIMROTH (1891), referring to two specimens of Arion- 
idae from Guarda (Portugal) sent by Mr. Paulino d’Olivei- 
ra, thought that externally they were very similar to Geo- 
malacus anguiformis, and that they were probably an 
intermediate form between it and G. maculosus. He de- 
scribed this species in detail, naming it Geomalacus oliveirae 
and comparing it to anatomically close species. wo years 
later SIMROTH (1893) commented that the description of 
this species showed that the Portuguese fauna, in relation 
to this new genus, had still not been fully researched. There 
are no more references to G. oliveirae until NOBRE (1941) 
stated that he knew no diagnosis for it. It is absent from 
SEIXAS’ (1976) account of the Portuguese fauna. 

In SIMROTH’s (1891, 1893) view the species of the genus 
Geomalacus are distributed along the mountain chains that 


The Veliger, Vol. 36, No. 2 


go from east to west across the Iberian Peninsula, and he 
stated that it was strange to find at least one of them, G. 
maculosus, along the southern rim of Ireland. According 
to Simroth, in Spain the northern species, G. maculosus, 
should appear in the Cantabrian cordillera, G. oliveirae 
should appear in the Castilian mountains, and G. angui- 
formis in the Betic system. In 1893 SIMROTH urged a study 
of the genus Geomalacus in order to make its taxonomic 
position clear and to demonstrate or disprove that it was 
separated by mountain chains. NOBRE (1941) did just that 
and attempted to study the species reported in Portugal; 
he merely stated that they were introduced species, since 
he could only find one specimen of G. maculosus. 


MATERIALS ano METHODS 


Specimens were gathered by day and night. During the 
day hiding places occupied by Geomalacus were sought, so 
that at night the slugs could be captured when they emerged 
or fed. Transport, fixing, conservation, and dissection were 
performed according to the methodology used by ADAM 
(1960) and CASTILLEJO (1981a). 

Scale drawings were made with the aid of a tracing 
screen attached to a binocular viewer. The scales in each 
drawing were calculated using a piece of paper with mil- 
limeter squares placed on the sample. 


RESULTS 


Specimens of the genus Geomalacus were collected at sev- 
eral sites in mainland Portugal, including the type localities 
of the species described in Portugal. It was also possible 
to study a specimen of G. maculosus found at Carugh Lake, 
in Ireland, and deposited in the British Museum (No. 
70.12.23.45). 

Drawing on the bibliographic data available to us con- 
cerning Geomalacus, not only for the Iberian Peninsula but 
also for the rest of Europe (no reference has ever been 
made to this species outside Europe), we consider that the 
differences, which Simroth used for separating G. macu- 
losus and G. grandis, are not significant differences and 
that G. maculosus and G. grandis are the same species, with 
the name G. maculosus having priority and G. grandis being 
a junior synonym. As regards G. anguiformis and G. olwwet- 
rae, we believe that both are good species. 

From the study of all the specimens collected in Portugal 
we have reached the same conclusion that we reached from 
studying the literature; namely that, these specimens can 
be assigned to three species: Geomalacus maculosus, G. an- 
guiformis, and G. oliveirae. 


Geomalacus maculosus Allman, 1843 
(Figures 1-13) 


Letourneuxia lusitana Silva & Castro, 1873 
Limax lusitanus Morelet, 1877 

Geomalacus lusitanus Pollonera, 1890 
Geomalacus grandis Simroth, 1893 


T. Rodriguez et al., 1993 


: Rot ? eH s 
SOTO a etre a ee 


eens: 


SE TTET 
aR i 
z ate “s ze 


Page 147 


a =e IR 


Pees 


Explanation of Figures 1 to 3 


Figures 1-3. Geomalacus maculosus. Dorsal, lateral, and ventral views of a specimen from the Serra da Estrela (type 


locality of Geomalacus grandis). Scale 5 mm. 


Description and iconography: Geomalacus grandis SIM- 
ROTH, 1893:291; pl. 1, fig. 1; pl. 2, figs. 1-3; NoBRE, 1930: 
65; pl. 1, fig. 4; NoBRE, 1941:74; pl. 2, fig. 4; CASTILLEJO, 
1981:105; pl. 15, 16; pl. 125, figs. 1-4, 6. Geomalacus 
maculosus Allman, 1843: ALLMAN et al., 1846:297, pl. IX; 
PLATTS & SPEIGHT, 1988:417, figs. 1-7. 


Material examined: Locations in Portugal (Figure 14): 
Sabugueiro (Serra da Estrela), 29TPE17, 28 March 1983, 
23 specimens; Sao Romao (Serra da Estrela), 29TPEO7, 
29 March 1983, 1 specimen; Ermita de Nossa Senhora do 
Desterro (Serra da Estrela), 29TPE17, 29 March 1983, 
14 specimens; Portela do Homem (Serra de Gerés), 
29TNG72, 9 March 1984, 1 specimen; Albergaria (Serra 


de Gerés), 29TNG72, 31 October 1984, 7 specimens; Cur- 
ral de Leonte (Serra de Gerés), 29TNG72, 1 November 
1984, 8 specimens; Quintas (Chaves), 29TPG10, 2 No- 
vember 1984, 1 specimen; Chaos (Guarda, Serra da Es- 
trela), 29TTPE48, 28 November 1984, 14 specimens, and 
29 November 1984, 2 specimens; Rabal (Braganga), 
29TPG83, 6 December 1985, 41 specimens; Sao Pedro do 
Sul, 29TNF71, 9 December 1985, 1 specimen; Vouzela 
(Sao Pedro do Sul), 29TNF70, 10 December 1985, 16 
specimens; Pacos (Sao Pedro do Sul), 29TNF70, 10 De- 
cember 1985, 1 specimen; Luso (Coimbra), 29TNE56, 11 
December 1985, 2 specimens, and 28 January 1986, 1 
specimen; Viana do Castelo, 29TNG11, 14 December 1985, 
16 specimens; Mirador de Sao Silvestre (Viana do Castelo), 
29TNG11, 15 December 1985, 3 specimens. 


The Veliger, Vol. 36, No. 


Page 148 


us ar biee, ES 


s St 


Explanation of Figures 4 to 8 
Figures 4-8. Geomalacus maculosus. Figure 4. Organs in situ. Figure 5. Digestive tract. Figure 6. Ocular retractor 


muscles. Figure 7. Limacella. Figure 8. Dorsal view of pallial complex. Scale 1 mm. 


T. Rodriguez et al., 1993 


Page 149 


ae ee wt! s 
: fs! 
Se. noe 
if ASHE 


itis 


Explanation of Figures 9 to 13 


Figures 9-13. Geomalacus maculosus. Figure 9. Genital apparatus. Figure 10. Interior of intermediate canal. Figure 
11. Interior of epiphallus. Figure 12. Interior of oviduct. Figure 13. Spermatophore. Scale 1 mm. 


Description: External morphology (Figures 1-3): Large 
slug, 120 mm long maximum, though normally only 70- 
80 mm (in vivo); length in 70% alcohol 60-70 mm. 

Body surface mottled white or yellow, for gray or green 
body color, respectively. Yellow mucus. White sole. In 70% 
alcohol, back yellowish green with some dark spots. 

Juveniles sometimes have two longitudinal lateral bands 
disappearing with age. 

Internal anatomy: (a) Digestive tract (Figure 5): Intestine 
with two circumvolutions. 


(b) Limacella (Figure 7): Solid, with clear nucleus, long, 
irregular in outline and width, growth lines just visible. 

(c) Genitalia (Figures 9-13): Atrium long, lined inter- 
nally by a series of longitudinal grooves. Vaginal diver- 
ticulum very long, slightly dilated around the atrium and 
lined inside by circular grooves, thus appearing festooned 
externally. 

Free oviduct short, covered inside by seven partially 
overlapping longitudinal grooves giving aspect of ligule. 

Bursa copulatrix rounded, with short duct; retractor 


Page 150 


anes 
. ‘ 
\ ye 
\ 
lee ee 
/ Be % 
ae “ 
| ,—~ 
ea \ 
ibe ie 
j ; 
LK | i 
Ns \ 
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\ pe 
ae 
(eee |) 
Figure 14 


Provisional distribution of Geomalacus maculosus in Portugal. 


muscle anchored inside, very long and inserting in caudal 
part of the animal, close to hermaphrodite gland. 

Epiphallus (Figure 11) large, rolled spirally and lined 
internally by many prefectly aligned papillae giving the 
appearance of longitudinal grooves visible externally. Vas 
deferens thinner and smaller. 

Ovotestis consists of dark colored groups of acini. 

In only one of the studied specimens were fragments of 
spermatophore found (Figure 13), so we can not describe 
spermatophore morphology. 


Habitats and distribution: The slug is crepuscular, dis- 
appearing during the day in gaps between rocks, in the 
earthy slopes, or under tree bark. This earthworm-like 
ability to hide in cracks is due to its flattened, uniformly 
wide body (only the lower part is slightly tapered) (PLATTS 
& SPEIGHT, 1988). 

SIMROTH (1891) recorded two characteristics of this spe- 
cies: one, the strange way that it curls when eating, such 
that the head and eyes protrude only slightly from beneath 
the mantle, and, the other, its reaction when caught, in 
which the lower part of the sole folds up to the upper part. 

Geomalacus maculosus can live on feeds supplemented 
with pieces of fungi and fresh vegetables (PLATTS & 
SPEIGHT, 1988). It does not seem to require a particular 
diet since it has been found to eat a wide variety of lichens 


The Veliger, Vol. 36, No. 2 


and liverworts (TAYLOR, 1907). In Portugal we captured 
G. maculosus browsing on lichens growing on granite and 
similar rocks, on walls surrounding fields, in cemeteries 
and on church walls; on some occasions it was found on 
schists, or greywackes (Brangang¢a), red sandstones, con- 
glomerates, or marls (Luso-Bugaco). In woods we found 
it on the mossy or lichen-covered barks of Quercus robur, 
Q. suber, Q. lusitanica, Castanea sativa, or Pinus pinaster. 

All the zones where it has been found have Atlantic 
climates, above 1000 mm mean annual precipitation and 
a mean annual temperature varying between 8°C in upland 
regions and 12°C in lowland. This species is common to 
all of northern Portugal down to the Mondego River and 
the Serra da Estrela. Its distribution is restricted to the 
Atlantic area of the Iberian Peninsula (north Portugal, 
Galicia, Asturias, and Santander) and the south of Ireland. 
It has been reported from Brittany, France, but we would 
not collect it there and thus its presence in France remains 
unconfirmed. 

PLATTS & SPEIGHT (1988) recommended the need to 
protect Geomalacus maculosus in Ireland, where it is a rare 
species. With regards to the fauna of northern Spain and 
Portugal, the species is fairly common and we collected 
many specimens in Santander, Asturias, Leon, Galicia, 
and the north of Portugal, finding, as did Platts & Speight, 
that the global distribution of this genus is restricted to 
the Lusitanian area. 


Discussion: In his description of Geomalacus grandis SIM- 
ROTH (1893) said that it is closely related to G. maculosus. 
In a synoptic table he noted the characteristics of the four 
species found in Portugal, showing that the only differences 
between G. maculosus and G. grandis are the size of the 
atrium and the length of the animal (in both cases G. 
grandis is bigger). It is a possible that the specimens of G. 
maculosus Simroth studied from Ireland were juveniles, 
which would explain his assignment of 40 specimens col- 
lected at the Serra de Gerés to G. maculosus and the as- 
signment two years later of sexually mature individuals to 
G. grandis. 

We had the opportunity of studying a topotype of Geo- 
malacus maculosus deposited in the British Museum (Lon- 
don), the external and internal anatomy of which coincide 
with the specimens we collected in northern Portugal. From 
this determination we are able to definitively synonymize 
G. grandis and G. maculosus. 


Geomalacus anguiformis (Morelet, 1845) 
(Figures 15-23) 


Limax anguiformis Morelet, 1845 

Limax squammantinus Morelet, 1845 

?Limax viridis Morelet, 1845 

Geomalacus anguiformis (Morelet, 1845): POLLONERA, 1890 

Geomalacus squammantinus (Morelet, 1845): POLLONERA, 
1890 

Geomalacus anguiformis (Morelet, 1845): SIMROTH, 1891 

Geomalacus anguiformis (Morelet, 1845): NOBRE, 1941 


T. Rodriguez et al., 1993 Page 151 


Fico aA OR oars, 


Explanation of Figures 15 to 18 


Figures 15-18. Geomalacus anguiformis. Figure 15. Lateral and dorsal views of a specimen from the Serra de 
Monchique (type locality of Geomalacus anguiformis). Figure 16. Organs in situ. 


Figure 17. Dorsal view of pallial complex. Figure 18. Limacella. Scale 1 mm. 


Page 152 


The Veliger, Vol. 36, No. 2 


ttra-- 


ToS eae ee 


TNs 


eB ye at 


SASSY 


Explanation of Figures 19 to 21 


Figures 19-21. Geomalacus anguiformis. Figure 19. Pallial complex. Figure 20. Ocular retractor muscles. Figure 


21. Digestive tract. Scale 1 mm. 


Description and iconography: Geomalacus anguiformis 
SIMROTH, 1891: 355; pl. 5, fig. 7; pl. 6, fig. 8; pl. 7, figs. 
2-2b. 


Material examined: Locations in Portugal (Figure 24): 
Marmelete (Serra de Monchique), 29SNB23, 15 April 
1984, 17 specimens; Caldas de Monchique (Serra de 


Monchique), 29SNB32, 15 April 1984, 19 specimens; Al- 
ferce (Serra de Monchique), 29SNB43, 16 April 1984, 20 
specimens; Monchique, 29SNB33, 16 April 1984, 15 spec- 
imens, and 2 December 1984, 12 specimens; Road Mon- 
chique-Foia, 29SNB32, 16 April 1984, 3 specimens; 
Barranco do Velho (Serra do Caldeirao), 29SNB92, 30 
November 1984, 24 specimens, and 1 December 1984, 8 


T. Rodriguez et al., 1993 Page 153 


p= ABE OB 


Explanation of Figures 22 and 23 


Figures 22, 23. Geomalacus anguiformis. Figure 22. Genital apparatus. Figure 23. Spermatophore (with the teeth 
enlarged). Scale 1 mm. 


Page 154 


—N . 
\ 


Nae 
SC 


y 
) 


} 
Se 


ee 


Figure 24 


Provisional distribution of Geomalacus anguiformis in mainland 
Portugal. 


specimens; Alportel (Serra do Caldeirao), 29SNB91, 1 
December 1984, 52 specimens, and 2 December 1984, 8 
specimens. 


Description: External morphology (Figure 15): Extended 
length 60-70 mm, not exceeding 50 mm in 70% alcohol. 

Body coloring very varied. Young juveniles blue-black 
with whitish tubercles; back with almost black bands; ju- 
veniles somewhat lighter, blue more prominent, masking 
the white of the dorsal tubercles, while bands broaden; 
adults chestnut color, yellow at body margins, the four 
dorsal bands dark chestnut, in some cases almost black; 
some specimens gray with black bands. 

Back grayish-brown in 70% alcohol, with four dark 
longitudinal bands; the two central bands reaching the 
shield. Sole whitish, lateral margins light. 

Internal anatomy: (a) Digestive tract (Figure 21): In- 
testine with two circumvolutions. 

(b) Limacella (Figures 17, 18): Oval, with inferior nu- 
cleus and light growth lines. 

(c) Genitalia (Figures 22, 23): Genital atrium large and 
cylindrical, in adults covered externally by glandular mass, 
in juveniles unmarked, lined internally by 7 to 12 recti- 
linear longitudinal grooves in both. Vaginal diverticulum 
short, cylindrical or spherical, smooth, with little internal 
grooving (papillous folds). 

Bursa copulatrix oval, bursa copulatrix duct very long, 


The Veliger, Vol. 36, No. 2 


entering, along with the epiphallus, in the vaginal diver- 
ticulum. Bursa retractor muscle long, connected at lower 
third of duct; folds into U- or L-shape where it enters 
duct. 

Free oviduct smaller than the genital atrium. Epiphallus 
tubular, dilated apically, 10-15 times larger than the ovi- 
duct, covered inside with serrated helicoidal or longitudinal 
grooving. Vas deferens shorter (by almost half) than the 
epiphallus. Epiphallus-vas deferens transition is indistinct. 

Spermoviduct well developed. Albumin gland large and 
whitish. Hermaphrodite gland long and slightly festooned. 
Ovotestis spherical, with darkish acini. 

Spermatophore (Figure 23) long, approximately 35 mm, 
square in cross section and provided with three longitu- 
dinal rows of non-helicoidal toothlets. Amber in color, 
lacking a set of teeth at one end. 


Habitats and distribution: In Portugal, Geomalacus an- 
guiformis occurs in areas of clayey schists, greywackes, and 
sandstones (Serra do Caldeirao) and on medium- to coarse- 
grained nepheline-syenites (Serra de Monchique). In both 
sierras, species of the genus Quercus dominate together 
with Olea oleaster, Pinus sp., Rhododendron ponticum, and 
Arbutus unedo. 

The Serra de Monchique exhibits a thermoatlantic cli- 
mate—z.e., always humid, sub-Mediterranean mesother- 
mic oceanic climate. In the Serra do Caldeirao the climate 
is Mediterranean. In both sierras, mean annual rainfall 
is about 1000 mm and the mean annual temperature about 
16°C. (ANONYMOUS, 1984). These sierras, especially the 
Serra de Monchique, represent the only green, humid 
zones in all the Portuguese Algarve. 

Although Geomalacus anguiformis is known only in the 
south of Portugal, it is very likely that it also occurs in the 
Spanish provinces of Badajoz and Huelva. As a species it 
is confined to the southeast of the Lusitanian area and 
found, at the moment, in the mountain chains of southern 
Portugal. 


Discussion: The specimens we collected show great vari- 
ation as regards color. This may be diet related, since the 
young juveniles and the juveniles were collected in the 
spring browsing on lichens on rocks (granite and schist), 
while adults, captured in the autumn, were feeding on 
toadstools in the woods of both sierras, consisting mostly 
of cork oak (Quercus suber) and Arbutus unedo. 

A comparison of our specimens with those sketched by 
SIMROTH (1891:pl. 3, fig. 8) revealed that the festoonery 
shown by this author on the vaginal diverticulum and in 
the bursa copulatrix duct are not found on any of the 
specimens we have dissected. This difference may be due 
to the method of preserving the animals, since Simroth 
himself stated that in November 1891 he collected 20 spec- 
imens of Geomalacus anguiformis on fungi in the Serra de 
Monchique and transported them alive to Lisbon, except 
for five specimens that he preserved in alcohol; it is possible 
that these specimens were already almost dead before being 
placed in alcohol. 

One of the specific names that we have synonymized is 


T. Rodriguez et al., 1993 


Limax viridis Morelet, 1845. The original description of 
this species stated that L. viridis has a blunted cowl on its 
back. This cowl is not characteristic of the Arionidae, and 
after considering the opinions of other authors such as 
POLLONERA (1890) and SIMROTH (1891) on Geomalacus 
anguiformis, the synonymy is in doubt, as indicated with 
a question mark. 

Geomalacus oliveirae Simroth, 1891, is closely related to 
G. anguiformis. It differs externally in that it is shorter. 
This difference is also seen in the genitalia, apart from 
the oviduct, which is slightly larger in G. oliveirae than in 
G. anguiformis. Geomalacus oliveirae was described from 
the Serra da Estrela (central-north Portugal) and G. an- 
guiformis was described from the two sierras of south Por- 
tugal. We have not captured any specimens of either species 
in the region between the southern and northern mountain 
chains. After comparing their genitals, finding that they 
are different, and confirming their geographical isolation, 
we consider that both species are distinct. 

Recently, WIKTOR & PAREJO (1989) redescribed Geo- 
malacus anguiformis with specimens collected in the prov- 
ince of Toledo (Spain). Their description does not agree 
with that of the G. anguiformis we collected in the Serra 
do Caldeirao and the Serra de Monchique (the type lo- 
cations for G. anguiformis), but it is in keeping with the 
specimens we captured in the Serra da Estrela and assigned 
to G. oliveirae. The taxonomic position of the species re- 
described by Wiktor & Parejo is discussed at a later point. 


Geomalacus oliveirae Simroth, 1891 
(Figures 25-31) 


Description and iconography: Geomalacus oliverrae SIM- 
ROTH, 1891:359; pl. 6, fig. 9. 


Material studied: Locations in Portugal (Figure 32): 
Guarda, 29TPE48, 28 March 1983, 1 specimen; Caldas 
de Manteigas, 29TPE27, 28 March 1983, 1 specimen; 
Chaos, 29TPE48, 28 November 1984, 5 specimens; Sa- 
meiro, 29TPE27, 29 November 1984, 1 specimen; cross- 
roads of Guarda-Manteigas with Gouveia, 29TPE17, 29 
November 1984, 1 specimen. 


Description: External morphology (Figures 25, 26): In vivo 
length does not exceed 45 mm, 30 mm in alcohol. Body is 
chestnut in color with four black bands. Body margins 
light colored. The two internal bands not totally contin- 
uous, interrupted at irregular intervals in most individuals. 
Sole white, tripartite with very narrow central zone. 

In 70% alcohol, body grayish-brown, with two darker 
longitudinal bands on either side of two other bands, also 
dark. Light lateral margins of body; sole whitish. 

Internal anatomy: (a) Digestive tract (Figure 27): Char- 
acteristic of the genus. 

(b) Limacella (Figure 28): Oval, with light inferior nu- 
cleus. Growth lines also light colored. 

(c) Genitalia (Figures 29-31): Genital atrium cylindri- 
cal, covered externally by a glandular mass only in adults, 


Page 155 


internally 7-9 longitudinal grooves. Vaginal diverticulum 
short and smooth. 

Bursa copulatrix rounded, with short, thick duct; cov- 
ered internally by a series of transverse grooves festooned 
with a paving-like design. Bursa and duct darkish. Before 
junction with epiphallus, the bursa copulatrix duct has an 
annular dilation covered internally by short, thick longi- 
tudinal grooves. 

Oviduct cylindrical, somewhat larger than atrium, lined 
with fine longitudinal grooves. Forms continuation of atri- 
um. 

Epiphallus cylindrical, slightly larger than vas deferens, 
lined with 7-9 longitudinal, festooned grooves. 

Retractor muscle enters close to bursa copulatrix. 

No spermatophore found. 

Spermoviduct well developed. Albumin gland whitish. 
Hermaphroditic duct lengthened and festooned. Ovotestis 
spherical, with darkish acini. 


Habitats and distribution: The area of Portugal where 
this species was found is granitic, with Mediterranean- 
type vegetation below 1300 m and Betula pubescens, Pinus 
sylvestris, and Juniperus communis above. A change with 
elevation is also seen in the climate, which above 1300 m 
is very wet, cold in winter, and warm in summer. The 
mean annual precipitation exceeds 2400 mm and the mean 
temperature is between 7.5 and 10°C. 


Discussion: The species is virtually unknown, since the 
only description is from 1891. Since then, it has been 
overlooked, not taken into account, or considered a syn- 
onym of Geomalacus anguiformis, a close species which 
differs in some respects, however. 

SIMROTH (1893) contrasted their characteristics in a 
table similar to the following: 


G. olwetrae G. anguiformis 


Atrium long long 

Atruim-penis lateral; short to the end of atri- 
um; medium 

Bursa duct long long 

Receptaculum rounded stretched out 

Proximal inser- close to the lung __ close to the poste- 

tion of retractor rior end of the 

body 


Distal insertion close to the bursa in the bursa duct 


We noticed the following differences: 


G. oliveirae G. anguiformis 


Atrium lengthened; pig- 
mented 7-9 lon- 
gitudinal inter- 
nal grooves 

Vaginal divertic- smooth or with 


ulum light nervations 


lengthened; pig- 
mented 9-10 
longitudinal in- 
ternal grooves 

7 thick grooves 


Page 156 


The Veliger, Vol. 36, No. 2 


Explanation of Figures 25 to 28 


Figures 25-28. Geomalacus olweirae. Figures 25, 26. Dorsal and lateral view of a specimen from the Serra da 
Estrela (type locality of Geomalacus oliveirae). Figure 27. Digestive tract. Figure 28. Limacella. Scale 1 mm. 


Bursa duct short and pig- large, twisted into 


mented around an L-shape 
the bursa 
Oviduct large short 
Muscle close to the bursa further away 
Epiphallus + vas 30-35 mm 50-60 mm 
deferens 
Bursa pigmented not pigmented 


The differences between the two species, although few, 
are constant, leading us to think that these species could 


be completely separate; to their anatomical distinctness we 
should add differences in vegetation, soil, and climate, 
along with a real geographical separation, since we have 
not captured any representatives of either species, nor any 
intermediate form in between the two southern ranges 
(Caldeirao and Monchique) and the northern (Serra da 
Estrela). 

As regards climate, the Serra da Estrela has a mean 
annual precipitation exceeding 2400 mm and a mean an- 
nual temperature of below 10°C, compared to the 1000 


T. Rodriguez et al., 1993 


Page 157 


Explanation of Figures 29 to 31 


Figures 29-31. Geomalacus oliweirae. Genital apparatus of three specimens from the Serra da Estrela. Scale 1 mm. 


mm and 16°C of the sierras of Caldeirao and Monchique. 
As regards the vegetation of the two sierras in the south 
(Caldeirao and Monchique) dominant species belong to 
the genus Quercus (Q. faginea, Q. lusitanica, Q. suber, Q. 
lex) together with Olea oleaster and Pinus pinea; in the 


Serra da Estrela we find Betula pubescens, Castanea sativa, 
Juniperus communis, Pinus silvestris, and Quercus pyrenaica. 
In the Serra da Estrela the soil contains high levels of 
aluminum, carbon, and nitrogen and low levels of mag- 
nesium, potassium, calcium, and sodium, while the soils 


Page 158 


Ee 


if 


Seale 


f if 
/ | eS) 
x 


Figure 32 


Provisional distribution of Geomalacus oliveirae in mainland Por- 
tugal. 


of the two southern sierras have high levels of magnesium, 
potassium, sodium, and calcium and low levels of alumi- 
num, carbon, and nitrogen. 

Curiously, the light pigmentation that appears in the 
bursa duct, the bursa, and the atrium of Geomalacus oliv- 
eirae also appeared in the species of the genus Avion that 
we found in the Serra da Estrela. 

As already stated, WIKTOR & PAREJO (1989) have re- 
described Geomalacus anguiformis with specimens collected 
in the province of Toledo (Spain). These specimens are of 
the same size as G. oliveirae; the bursa copulatrix duct is 
short, as is the retractor muscle; and the epiphallus and 
vas deferens together, in both cases, do not exceed 35 mm 
in length. In contrast, as already mentioned in the discus- 
sion of G. anguzformis, the specimens of the Serra do Caldei- 
rao and Serra de Monchique have a large bursa copulatrix 
duct, folded into an L-shape, and the retractor muscle is 
just as long, entering at the caudal part of the animal; 
furthermore, the epiphallus and vas deferens are, together, 
twice as long as those found in G. olivezrae, exceeding 60 
mm in most of the specimens dissected. 

From all that has been said, we believe that the report 
from Toledo corresponds to Geomaculus oliveirae and not 
to G. anguiformis, which represents the first sighting of G. 
oliverrae for Spain. But this will only be confirmed when 


The Veliger, Vol. 36, No. 2 


the Iberian Peninsula is sampled systematically from the 
center down, to see whether there is continuity in the 
distribution of these two species in the sierras of the center 
and south of the peninsula. 


ACKNOWLEDGMENTS 


We thank the British Museum for letting us study a mor- 
photype. We also thank Dr. Wiktor (Poland) for his opin- 
ions and advice and for the critical revision of the material 
utilized in this manuscript. 


LITERATURE CITED 


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dulcicolas. Institut Royal des Sciences Naturelles de Bel- 
gique: Bruxelles. 402 pp. 

ALLMAN, G. J. 1843. Ona new genus of terrestrial gasteropod. 
The Athenaeum. 851. 

ALLMAN, G. J. et al. 1846. Description of a new genus of 
pulmonary gasteropods. The Annals and Magazine of Nat- 
ural History 113:297-299. 

ANONYMOUS. 1984. Portugal. Atlas do Ambiente. Carta de 
Temperatura. Carta de Precipitagao. Comissao Nacional do 
Ambiente: Lisbon. 

CASTILLEJO, J. 1981. Los moluscos terrestres de Galicia (Sub- 
clase Pulmonata). Doctoral Thesis, Universidad de Santiago. 
515 pp. 

CASTILLEJO, J. 1981b. Los pulmonados desnudos de Galicia. 
I. Geomalacus grandis Simroth, 1893 (Gastropoda, Arioni- 
dae). Iberus 1:53-60. 

CASTILLEJO, J. & M. Y. MANGA. 1986. Notes on some slugs 
(Mollusca, Stylommatophora) in the N.W. part of the Ibe- 
rian Peninsula. Proceedings of the 8th International Mal- 
acological Congress Budapest, 1983. Pp. 43-48. 

GERMAIN, L. 1930. Mollusques terrestres et fluviatiles, 1-2. 
Faune de France. Paris. 897 pp. 

HIDALGO, J. G. 1916. Datos para la fauna espanola (Moluscos 
y Braquidpodos). Boletin de la Real sociedad Espanola de 
Historia Natural (Biologia) 16:235-246. 

MoRELET, A. 1845. Description des mollusques terrestres et 
fluviatiles du Portugal. J. B. Bailliére: Paris. 177 pp. 
MOoRELET, A. 1877. Revision des mollusques terrestres et flu- 
viatiles du Portugal. Paris. Journal de Conchyliologie 21:1- 

24. 

NosreE, A. 1930. Moluscos terrestres, fluviais e das aguas sa- 

lobres de Portugal. Ministerio de Agricultura, Porto. 259 


PP. 

Nosre, A. 1941. Fauna malacologica de Portugal. II. Moluscos 
terrestres e fluviais. Coimbra. 277 pp. 

OUTEIRO, A. 1988. Gasteropodos de O Courel. Lugo. Doctoral 
Thesis, Universidad de Santiago. 626 pp. 

PiaTts, E. & M. C. D. SPEIGHT. 1988. The taxonomy and 
distribution of the kerry slug Geomalacus maculosus Allman, 
1843 (Mollusca, Arionidae) with a discussion of its status 
as a threatened species. The Iris “Naturalists” Journal 22(10): 
417-430. 

POLLONERA, C. 1890. Recensement des Arionidae de la Region 
Paléarctique. Bolletino dei Musei di Zoologia ed Anatomia 
comparata della Universita di Torino 87(5):1-40. 

Quick, H. E. 1960. British slugs (Pulmonata, Testacellidae, 
Arionidae, Limacidae). The Bulletin of the British Museum 
(Natural History) Zoology 6(3):105-226. 

SEIxAS, M. M. P. 1976. Gasteropodes terrestres da fauna por- 


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tuguesa. Boletim da Sociedade Portuguesa de Ciéncies Na- 
turais 16:21-46. 

Sitva, A. L. DA & J. DA CasTRO. 1873. Mollusques terrestres 
et fluviatiles du Portugal. Espéces nouvelles ou peu connues. 
Journal de Sciencies Mathematicas, Physicas e Naturales 
15:241-246. 

SIMROTH, H. 1891. Die nacktschnecken der portugiesisch-azo- 
rischen fauna in ihrem Verhdltniss zu denen der palaark- 
tischen region Uberhaupt. Nova acta. 424 pp. 

SIMROTH, H. 1893. Beitrage zur Kenntniss der portugiesischen 


Page 159 


und der ostafrikanischen Nacktschnecken-fauna. Abhand d. 
senckenb naturforsch Gesellesch 18:289-309. 

TayLor, J. W. 1907. Monograph of the land and freshwater 
Mollusca of the British Isles. Parts. 13, 14, 22-24. Taylor 
Brothers: Leeds. 640 pp. 

WIkToR, A. & C. PAREJO. 1989. Geomalacus (Arrudia) angui- 
formis (Morelet, 1845), its morphology and distribution. 
(Gastropoda, Pulmonata: Arionidae). Malakologische Ab- 
handlungen Staatliches Museum ftir Tierkunde Dresden 
14(3):15-25. 


The Veliger 36(2):160-165 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


The Taxonomic Status of Buccinanops dOrbigny, 
1841 (Gastropoda: Nassariidae) 


GUIDO PASTORINO 


Division Paleozoologia Invertebrados, Museo de Ciencias Naturales, 
Paseo del Bosque s/n, 1900 La Plata, Buenos Aires, Argentina 


Abstract. The radulae of Buccinanops cochlidium (Dillwyn, 1817) and B. moniliferum (Kiener, 1834) 
were observed for the first time using the scanning electron microscope. Radular, morphological, and 
reproductive characters of the genera Bullia, Dorsanum, and Buccinanops are compared. It is concluded 
that the South American species belong to the genus Buccinanops. 


INTRODUCTION 


Species of the genus Buccinanops d’Orbigny, 1841, have 
been considered as belonging to several different taxa in 
previous works. Table 1 shows the genera and subgenera 
to which these species have been assigned by previous 
authors. 

Seven species are presently included in the genus Buc- 
cinanops, all of them endemic to South America (see Table 
2). Members of Buccinanops live in soft bottomed, shallow 
waters of the intertidal or infralittoral zones. They gen- 
erally live in dense groups, and most of the species are 
scavengers. 

The aim of this paper is to reinstate Buccinanops to full 
generic status within the family Nassariidae. It was com- 
pared with Bullia Gray in GRIFFITH & PIDGEON, 1834, 
and with Dorsanum Gray, 1847, because they are similar 
in shell morphology. Radular, morphological, concholog- 
ical, and reproductive features were used for this compar- 
ison. 


MATERIALS anpD METHODS 


Radular studies were carried out on two species of Buc- 
cinanops: B. cochlidium from the localities detailed in Table 
3, and B. moniliferum from Praia de Pereque (Guaruja, 
Sao Paulo, Brazil). The radulae of both species were treat- 
ed following the method of SOLEM (1972) and observed 
under the SEM in the Museo de Ciencias Naturales, La 
Plata, Argentina (MLP). Specimens of all species of Buc- 
cinanops were also used from the malacological collection 
housed in the Division Zoologia Invertebrados (MLP). 


RESULTS 
Radula 


Buccinanops cochlidium has a rachiglossan radula (Fig- 
ures 4-6). The central tooth is multicuspidate with 5-11 
cusps that increase in size towards the middle of the series. 
The rachidian base is strongly curved when compared to 
the other species of the genus. 

The inner and outer cusps of the lateral teeth are hook- 
shaped. The first cusp may be bifid (Figure 4). The lateral 
teeth always have 1-3 intermediate cusps. Generally, the 
lateral teeth are symmetrical, but in some cases there is a 
peculiar asymmetry in the number and shape of cusps 
(Figure 4). 

The number of cusps (5-11) in the rachidian teeth of 
Buccinanops cochlidium represents the main variation. In 
addition, one or two prominent central cusps were also 
observed. There is no relation between the number of 
cusps, age, and sex (see Table 3). 

The radula of Buccinanops moniliferum is similar to that 
of B. cochlidium (Figures 1-3). The central tooth has 11 
cusps that decrease in size towards the sides. The rachidian 
base is gently concave with sharp borders. A more con- 
spicuous central cusp may be present. The lateral teeth 
have two hooked cusps with 1-4 intermediate cusps. 


Operculum 


Operculum morphology in all Buccinanops species is 
very uniform. The operculum is large, sub-oval, and smooth 
margined, and has a subterminal nucleus. The growth lines 
are well defined. 


G. Pastorino, 1993 


Page 161 


Table 1 


Genera and subgenera in which South American species of Buccinanops were placed by previous authors. 


Buccinanops 
COSSMANN (1901) 
STREBEL (1906) 
PEILE (1937) 
CARCELLES & PARODIZ (1939) 
CARCELLES (1944, 1950) 
CARCELLES & WILLIAMSON (1951) 
BARATTINI & URETA (1960) 
KLAPPENBACH (1961) 
CASTELLANOS (1970) 
Rios (1970, 1975) 
SCARABINO (1977) 
CERNOHORSKY (1984) 
Rios (1985) 
CALvo (1987) 


Buccinum 

DILLWYN (1817) 

KING & BRODERIP (1832) 

KIENER (1834) 

D’ORBIGNY (1841) 

DESHAYES in DESHAYES & EDWARDS (1844) 
Bullia 


REEVE (1846-1847) 

PILSBRY (1897) 

IHERING (1907) 

CERNOHORSKY (1982) 

ABBOTT & DANCE (1983, 1986) 


Shell 


In general, the shell is large and thick, with an oblique 
plait at the base and a carina behind the fasciole. It lacks 
ornamentation except for growth lines; however, some spe- 
cies have sharp tubercles on the subsutural shoulder of the 
last whorls (Buccinanops moniliferum (Kiener)), subsutural 
spiral lines (B. uruguayense (Pilsbry)), or axial ribs on the 
first three or four teleoconch whorls (B. cochlidium (Dill- 
wyn)). The apex is large, short, and blunt. 


Bullia (Buccinanops) 


ADAMS & ADAMS (1853) 
CHENU (1859) 
TRYON (1882) 
THIELE (1929) 
CERNOHORSKY (1982) 
ALLMON (1990) 

Dorsanum 
COSSMANN (1901) 
CARCELLES & PARODIZ (1939) 
CARCELLES (1944) 
BARATTINI & URETA (1960) 
CASTELLANOS (1970) 
Rios (1970, 1975) 
SCARABINO (1977) 


Buccinanops (Dorsanum) 
Rios (1985) (only for B. moniliferum) 


Egg Capsules 


The egg capsules of all known species of Buccinanops 
show the same morphological pattern (PENCHASZADEH, 
1971a, b, 1973). The capsules are attached to the callus 
and adjacent area of the mother’s shell by means of a short 
pedicle. More than 80 capsules are attached to several 
specimens of B. cochlidium. The capsules, which are oval, 
flattened, and clear, vary in size, form, and ornamentation 
according to the species. 


Table 2 


Recent species of Buccinanops d’Orbigny, 1841. Institutional abbreviations: ZMC—Zoological Museum, Copenhagen, 

Denmark; BM—British Museum (Natural History), London, England; MHNG—Muséum d Histoire Naturelle, Geneva, 

Switzerland; MN—Museo Nacional de Historia Natural, Montevideo, Uruguay; ANSP—Academy of Natural Sciences, 
Philadelphia, USA. 


Species and author Year 
B. cochlidium (Dillwyn)* 1817 
B. deforme (King & Broderip) 1832 
B. moniliferum (Kiener) 1834 
B. paytense (Kiener)t 1834 
B. globulosum (Kiener) 1834 
B. uruguayense (Pilsbry) 1897 
B. duarte: Klappenbach 1961 


* = B. gradatum (Deshayes in Deshayes & Edwards, 1844). 
+ = B. squalidum King & Broderip, 1832, non Gmelin, 1791. 


Type locality and repository 


Islands of South Seas. ZMC 

Gorriti, Argentina. BM1985003 

Terra Nova [sic]. ? 

Payta, Peru. ? 

?. MHNG1296/17/1 

Maldonado Bay, Uruguay. ANSP70504 
La Coronilla, Uruguay. MN0709 


Page 162 The Veliger, Vol. 36, No. 2 


Explanation of Figures 1 to 6 


Figures 1-6. Genus Buccinanops. Scanning electron micrographs of radulae. Figure 1. B. moniliferum, general view; 
scale bar = 500 wm. Figure 2. Detail of rachidian teeth of the specimen in Figure 1; scale bar = 100 um. Figure 
3. B. moniliferum, detail of rachidian teeth; scale bar = 500 um. Figure 4. B. cochlidium, arrowhead bifid cusps of 
the lateral tooth in asymmetric position; scale bar = 500 um. Figure 5. B. cochlidium, general view; scale bar = 
500 um. Figure 6. B. cochlidium, detail of rachidian teeth; scale bar = 100 um. 


G. Pastorino, 1993 


Page 163 


Table 3 


Radular and opercular parameters of Buccinanops cochlidium (Dillwyn, 1817). 


Operculum 
Shell length length 
(mm) (mm) Rachidian cusps __ Lateral cusps Sex Locality 
78 23.3 9 5 F Pto. Piramide, Chubut 
68.7 2G 8 5 F Pto. Piramide, Chubut 
90.8 30 7 4 F Pto. Piramide, Chubut 
49 16.6 11 5-4 F Pto. Piramide, Chubut 
91 29 8 4 F Rawson, Chubut 
60.3 18.4 6 4 F Rawson, Chubut 
59.2 21.6 6 5-4 M Rawson, Chubut 
78.8 28.5 8 5 F Mar del Plata, Buenos Aires 
TBD 26 9 4 F Mar del Plata, Buenos Aires 
63.2 24.3 9 4 F Mar del Plata, Buenos Aires 
79.2 26 5 + F Mar del Plata, Buenos Aires 
48.6 16 6 4 M Pto. Piramide, Chubut 
56 19 8 4 F Pto. Piramide, Chubut 
47 15.5 v 4 M Pto. Piramide, Chubut 
25.4 7.8 7 4 M Pto. Piramide, Chubut 
48.8 5 E2 6 4 F Pto. Piramide, Chubut 
45.3 14.9 1 4 M Pto. Piramide, Chubut 
75) 8.3 7 4 F Pto. Piramide, Chubut 
15.4 4.6 9 4 F Pto. Piramide, Chubut 
Larval Development contrast, the species of Budlia form a very heterogeneous 
Buccinanops species with known larval development have oe (ANIONS PD Dorsanum, Ropmese nee, ean On) 
one to nine embryos (B. cochlidium) that hatch in the py 2 eg (Eun) (Gang NEMO 0) snows 8 
Been feoeitionevecvcachl capsule’ may have up to very different set of features. Table 4 shows characteristic 
1600 nurse eggs (PENCHASZADEH, 197 1a, b, 1973). fearnessof ithe three Cees : 
The radulae characteristic of the three genera differ. 
DISCUSSION According to PEILE (1937), ADAM & KNUDSEN (1985), 
CALVO (1987), CERNOHORSKY (1984), and ALLMON (1990), 
Despite minor specific differences among Recent species rachidian teeth in Bullia and Buccinanops have similar 
of Buccinanops, they form a very homogeneous group. In morphology. Buccinanops, however, presents cusps that 
Table 4 


Comparison of generic features among Buccinanops, Dorsanum, and Bullia. 


Buccinanops 
Shell Large, with the base of the colu- 
mella with one oblique plait; 
large and blunt apex 
Animal Very large, with one posterior 
metapodial tentacle, without 
eyes, long cephalic tentacles 
Operculum Large, always without serrations, 
subterminal nucleus 
Larval Young hatch as crawling veliger, 
development only 1-9 eggs develop, others 


Egg capsule 


Radula 


used as nurse eggs 

Attached to the callous region of 
the female shell by means of a 
short pedicle 

Central tooth with cusps increas- 
ing in size towards the center 


Dorsanum 


Medium to small size siphonal 
channel bordered by two spiral 
ridges; small and multispiral 
apex 

Medium in size without posterior 
metapodial tentacles, with eyes, 
short cephalic tentacles 

Small, with smooth margins 


Young hatch as pelagic veligers, 
all eggs develop 


Always attached to the substrate 
Central tooth with cusps of the 


same size, lateral teeth always 
bicuspidate 


Bullia 


Medium to small size, more slender; 
without periostracum; acute apex 


Very large, with two posterior meta- 
podial tentacles, without eyes, 
long cephalic tentacles 

Small, some with marginal serra- 
tions 

Same as Buccinanops or ovovivipa- 
rous 


Some with filaments retained within 
the fold of the female’s foot or 
buried below sand surface 

Central tooth with cusps of the 
same size or subequal 


Page 164 


The Veliger, Vol. 36, No. 2 


decrease in size towards the sides, with one or two central 
prominent cusps (Figures 4-6). Bullia shows rachidian 
cusps of the same or sub-equal size. Dorsanum, too, has 
similar rachidian teeth, although the cusps are smaller than 
in the other genera and they are all the same size. 

The lateral teeth in Bullia show a great variety in num- 
ber and morphology. Usually they have one or two inter- 
mediate cusps. Buccinanops always presents more than one 
intermediate cusp, up to three in the observed specimens. 
Dorsanum always has a bicuspidate lateral tooth. 

Buccinanops and Bullia bear a carina posterior to the 
fasciole and a pronounced terminal columellar fold 
(CERNOHORSKY, 1984; ALLMON, 1990). Dorsanum, in con- 
trast, has two oblique spiral carinae bounding a reflexed 
siphonal channel around the anterior end of the fasciole. 
These features definitely set Dorsanum apart from the other 
two genera. The shell apices of Bulla and Dorsanum are 
more acute and slender than those of Buccinanops (ac- 
cording to ALLMON, 1990:plates 5, 6). 

Representatives of Buccinanops from studied localities 
are blind, have a well developed foot with one metapodial 
tentacle, and have large cephalic tentacles. Bullia is blind 
also, has two metapodial tentacles, and has long and slen- 
der cephalic tentacles (ALLMON, 1990). Once again, Dor- 
sanum differs significantly from the other two genera: it 
has true eyes, no metapodial tentacles, and short cephalic 
tentacles (ADAM & KNUDSEN, 1985). 

Opercula in Buccinanops cochlidium (Table 3), as in 
other species of the genus, are generally large with smooth 
margins. They vary little within the genus but differ great- 
ly from those of the other genera. In Bullia the operculum 
is always small, but may be serrated or smooth margined. 
In Dorsanum the operculum is small and smooth margined. 

Larval development in Bullia and Buccinanops shows 
several similarities, such as nurse eggs, non-planktonic 
larvae, and young that hatch as crawling veligers. How- 
ever, the egg capsules are very different. The egg capsules 
in most species of Bullia are carried on the ventral surface 
of the maternal foot (ALLMON, 1990); the egg capsules are 
oval, thin, and transparent with two threads at either end. 
In contrast to the situation in Bulla and Buccinanops, 
Dorsanum has egg capsules attached to the substrate, pe- 
lagic veligers, and no nurse eggs. 

ALLMON (1990) considered Buccinanops to be a sub- 
genus of Bullia on the basis of three factors: (1) The ranges 
of their conchological variations overlap; (2) They have 
non-planktonic larval development and are blind; and (3) 
Bullia, from South Africa and India, was judged to be the 
direct descendant of Buccinanops from South America. The 
first two factors are correct, although when compared to 
all the distinguishing features discussed in this paper there 
is supporting evidence to consider these genera as being 
distinct. Furthermore, the geographic distributions of Bul- 
lia and Buccinanops suggest two isolated lines of evolution. 
The idea of South African and Indian Bullia deriving from 
a South American ancestral stock of Buccinanops is prob- 


ably correct, but that fact is an insufficient reason to sub- 
ordinate Buccinanops to Bullia. 

According to many characters, having to do with the 
radula, shell, developmental mode, egg capsule, opercu- 
lum, and distribution, all the species of Buccinanops form 
an homogeneous group that differs substantially from the 
species of Bullia. Considering all of these, I suggest that 
Buccinanops be accorded full generic status. 


ACKNOWLEDGMENTS 


I wish to acknowledge the critical reading of the manu- 
script and constant encouragement of C. Ituarte and the 
valuable suggestions of A. C. Riccardi. W. Allmon kindly 
provided an up-dated bibliography. The Brazilian speci- 
mens were provided by J. C. Tarasconi. M. L. Pastorino 
supported the collection of the Argentine specimens. I. 
Finet from the Natural History Museum of Geneva, Swit- 
zerland, provided useful data about type specimens of Buc- 
cinanops. Finally I wish to especially acknowledge M. 
Griffin’s help with early versions of the manuscript. 
This work was carried out during the tenure of a schol- 
arship granted by the Consejo Nacional de Investigaciones 
Cientificas y Tecnicas (CONICET), Argentina. 


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The Veliger 36(2):166-173 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Formation of Organic Sheets in the Inner Shell 


Layer of Geloina (Bivalvia: Corbiculidae): 


An Adaptive Response to Shell Dissolution 


by 


SHINJI ISAJI 


Geological Institute, University of Tokyo, Hongo 7-3-1, Bunkyo-Ku, Tokyo 113, Japan 


Abstract. 


Two corbiculids, Geloina erosa (Solander) and G. expansa (Mousson), from the mangrove 


swamps of Iriomote Island, southern Japan, occasionally secrete 1-2 wm thick, periostracum-like organic 
sheets in the inner shell layer. In both species, the organic sheets occur only in specimens which have 
suffered extensive shell dissolution. Dissolution and organic sheets are especially common in the umbonal 
region. Numerous microtubes penetrate the inner shell surface in the umbonal region. These microtubes 
do not extend to the outer shell surface. Each microtube contains soft tissue which seems to perform a 
sensory function. Such organic sheets are not observed in the shells of other corbiculids living in normal 
brackish to freshwater environments. The organic sheets in the inner shell layer appear to protect the 
shell from dissolution. The formation of internal organic sheets in Geloina thus can be interpreted as 
an adaptive response to the acidic mangrove environments, where shell dissolution occurs easily. 


INTRODUCTION 


Recent corbiculids are euryhaline species occurring in the 
estuarine and lake environments of brackish to freshwater 
settings. Most corbiculids develop a thick periostracum to 
protect the shell from dissolution by acidic water in their 
habitats. Shell dissolution occurs easily when the perios- 
tracum has worn away from the shell surface. In fact full- 
grown specimens of most corbiculids have suffered shell 
dissolution in their umbonal region. Shell dissolution of 
bivalves inhabiting acidic environments have been studied 
by several workers (GRIER, 1920; TEvESZ & CARTER, 
1980; KaT, 1982, 1983; HINCH & GREEN, 1988). Some 
bivalve species suffering extensive shell dissolution have 
organic sheets in their shells. Several workers suggested 
that these organic sheets appear to protect the shell from 
dissolution (TAYLOR et al., 1969; LEwy & SAMTLEBEN, 
1979; TEVESZ & CARTER, 1980; KaT, 1982, 1983, 1985). 

Geloina is one of the characteristic corbiculids living in 
mangrove swamps of tropical to subtropical regions. Spe- 
cies of this genus live in waters having low pH, high 
temperature, and wide fluctuations in salinity (MORTON, 
1975, 1976). They can resist exposure for relatively long 
periods of time (more than two weeks; MorTON, 1976). 
Because of the acid soil of mangrove swamps, shell dis- 
solution of Geloina occurs more extensively than in cor- 


biculids living in other brackish to freshwater environ- 
ments. Geloina has several peculiar shell features, such as 
a heavy and thick shell, a thick periostracum, and inner 
periostracum-like organic sheets. These features are in- 
terpreted as adaptations to prevent shell dissolution. In 
this paper, I describe the microscopic features of the inner 
shell layer of Gelozna and the degrees of shell dissolution 
in relation to the bivalve’s habitats. I also propose a mech- 
anism for the formation of the internal organic sheets as 
a response to shell dissolution. 


Habitats of Geloina and 
Description of Collection Site 


Worldwide, the two major mangrove systems are in the 
Caribbean and the Indo-Pacific regions. The corbiculid 
clam Geloina occurs in mangrove-dominant brackish-water 
environments in the Indo-Pacific region, ranging from New 
Zealand to the Okinawa Islands (Japan) (MorTON, 1983). 
PRASHAD (1932) classified the Indo-Pacific Geloina into 
three species: G. erosa (Solander), G. bengalensis (La- 
marck), and G. expansa (Mousson). Later, MORTON (1983), 
who reexamined Geloina species throughout the Indo-Pa- 
cific region, supported PRASHAD’s (1932) view. 

This paper deals with two species of Geloina, G. erosa 
and G. expansa, living in mangrove swamps of Iriomote 


S. Isaji, 1993 


Page 167 


lriomote 
Island 


| 
RITAUR 


mudflats 


— mangrove Swamps 


0 1 2km 
eS 


Figure 1 


Map showing collecting localities for Geloina erosa and G. expansa. RITAUR; Research Institute of Tropical 
Agriculture, University of the Ryukyus. Site A: locality of the specimens without shell dissolution. Site B: locality 


of the specimens with extensive shell dissolution. 


Island, southern Japan. They occur in two different hab- 
itats, represented by sites A and B (Figure 1). At site A, 
during the low spring tides on 24 July 1992, the salinity 
was 23.2%. After a heavy rainfall (28 July 1992), the 
salinity was considerably decreased (to 4.9%o0). The pH 
values of surface and interstitial waters were measured in 
the two sites at the low spring tides on 29 July 1992 (Table 
1). The pH values of surface and interstitial waters at site 
A were 7.23-7.79 and 6.99-7.24, respectively. The sedi- 
ment is composed mainly of sand, gravel, and fragments 
of marine mollusks and corals, but contains no humus. 
The water is clear. Adjacent lithology is the Pleistocene 
Ryukyu limestone. No living specimens found at this site 


show evidence of shell dissolution in the umbonal region 
(Figure 2C). 

Compared to site A, site B has consistently high salinity 
and low pH. At the low spring tides on 24 July 1992, the 
salinity at this site was 27.7%o. Even after a heavy rainfall 
(28 July 1992), the salinity was 24.8%. The pH values 
of surface and interstitial waters were 6.99-7.13 and 5.06- 
6.54, respectively. At this site, small creeks contain small 
stagnant pools colored by organic matter. The sediment is 
composed of muddy, fine sand mixed with humus; it lacks 
fragments of marine mollusks and corals. Occasionally, 
small creeks and pools dry out in the landward edge when 
rainfall is low, suggesting that the landward edge in this 


Table 1 


Physico-chemical settings of the habitat of Gelozna on Iriomote Island, southern Japan (site A, site B). The pH values of 
surface and interstitial waters were measured at the low spring tides on 29 July 1992. 


pH of surface pH of interstitial 


sand, gravel, fragments of marine mol- 


Sediment type Adjacent lithology 


limestone (Ryukyu Lime- 


lusks, and corals without humus stone) 


water water 
Site A 7.23-7.79 6.99-7.24 
Site B 6.99-7.13 5.06-6.54 


muddy fine sand with humus 


sandstone and shale (Yae- 
yama Group) 


Page 168 


The Veliger, Vol. 36, No. 2 


Figure 2 i 


Geloina erosa. A and B. Specimen (UMUT RM 19106) from site B, showing extensive dissolution on the outer 
shell surface. Organic sheets are exposed in the umbonal region. C. Specimen (UMUT, RM 19107) without 
extensive shell dissolution from site A. D. Organic sheets in the umbonal region. Same specimen as in A and B. 
Scale bar: 1 mm. E and F. Organic sheets and microtubes (arrow) on etching surface. Same specimen as in D. 


Scale bar: 50 um. o, organic sheet. 


site is rarely covered by seawater. Adjacent lithology is 
sandstone and shale of the Miocene Yaeyama Group. All 
living specimens collected from this site have suffered 
marked shell dissolution in the umbonal region. Specimens 
occurring in the landward edge, where the duration of 
desiccation is longer, have suffered deep shell dissolution 
(Figure 2A, B). 


The differences in pH of the water between the two 
sites are consistent with the degrees of shell dissolution. 
Acidification of the waters in the mangrove swamps is due 
to acid sulfate soils and humic acid from humus. It appears 
to be affected by the duration of dry out and the content 
of humus. Therefore, long periods of desiccation and high 
humus content are related to low pH and shell dissolution 


S. Isaji, 1993 


Figure 3 


Scanning electron micrographs showing organic sheets in the inner shell layer of Geloina erosa (A-C)—same specimen 
as in Figure 2A—and Geloina expansa (D-F)—specimen (UMUT RM 19108) from site B. A and B, D and E. 
Fractured sections of organic sheets. C. Outer surface of organic sheet. F. Inner surface of organic sheet (mold). 
Depositional surface is toward the lower. cl, crossed-lamellar layer; 0, organic sheet. Scale bar: 10 wm. 


in Geloina at site B. On the contrary, fragments of marine 
mollusks, corals, and limestone present in the sediment 
appear to buffer the acidic condition of water, which seems 
to be undersaturated with calcium carbonate at site A. 


MATERIALS anD METHODS 


Living specimens of Geloina erosa and G. expansa were 
collected from two locations in the estuaries of the Hinai 
River, northern Iriomote Island (Figure 1A, B). After 


removing the soft tissue, shells of selected specimens were 
cut along the umbo-ventral margin, polished, and etched 
with 5% HCl. Small pieces of the etched shell were coated 
with platinum, and the internal shell structure was ex- 
amined by scanning electron microscopy (SEM). SEM 
observations were also made on fractured shell pieces that 
were neither polished nor etched. Acetate peels were pre- 
pared for etched shell cross sections and studied by optical 
microscopy. All specimens examined are deposited in the 
University Museum, University of Tokyo (UMUT). 


Page 170 The Veliger, Vol. 36, No. 2 


‘ ie 


Figure 4 
Scanning electron micrographs showing microtubes in the inner shell layer of Geloina expansa (A, B) and G. erosa 
(C-H). A and B. Fractured sections of microtubes. Same specimen as in Figure 3D-F. C. Organic sheet, which 


is curved into a microtube. Same specimen as in Figure 2D-F. D. Microtube located near the inner shell surface. 
UMUT RM 19109. E. Enlarged view of prismatic wall of the microtube in Figure 4D. F. Openings of microtubes 


S. Isayji, 1993 


Page 171 


Periostracum 
54 Outer finely crossed-lamellar layer 


Inner complex crossed-lamellar layer 


Dissolved surface ~~~. 


/ 
/ 


Figure 5 


Schematic cross section of the right valve of Geloina erosa cut along the line in Figure 2A, showing the position of 


organic sheets and microtubes. 


OBSERVATIONS 


The shell of the two Geloina species examined consists of 
an outer layer with a finely crossed-lamellar structure and 
an inner layer with a complex crossed-lamellar structure, 
with either an indistinct or thin prismatic pallial myos- 
tracum, as in other corbiculid shells (TAYLOR et al., 1973). 

In the specimens with marked shell dissolution in the 
umbonal region, several periostracum-like organic sheets 
occur in the inner shell layer. The eroded surface of the 
umbonal region exposes the organic sheets (Figure 2B, D). 
Therefore, shell dissolution appears to stop temporarily at 
these organic sheets (Figure 2E). 

The organic sheets are 1-2 um in thickness and occur 
at irregular intervals ranging from 150 to 500 um through 
the shell. The organic material shows a homogeneous 
structure in the fractured section. In having a homogeneous 
structure, the organic sheets are very similar to the peri- 
ostracum (Figure 3), although the periostracum has a sub- 
layer of vacuoles in the middle part (S. Isaji, unpublished 
data). These organic sheets are much thicker than the 
intercrystalline conchiolin layers, which are not observable 
using SEM on etched cross sections (Figure 2E, F). The 
outer surface of the organic sheets is flat with a more or 
less fine granular microstructure (Figure 3C). The inner 
surface is, in contrast, irregular in shape, with numerous 
hemispherical granules, about 0.5-2 wm in diameter and 
0.2-0.5 um in height (Figure 3F). The shell structure 
below the organic sheet has a homogeneous or prismatic 
structure (5-10 wm thick) (Figure 3A, B, D, E). 

When organic sheets are present in the inner shell layer, 
they always occur in the umbonal region, where extensive 


shell dissolution occurs. In highly eroded specimens, the 
hinge plate shows numerous organic sheets (Figure 5). For 
example, one such specimen was observed to have 10 or- 
ganic sheets in the umbonal region and 18 organic sheets 
in the hinge plate. These sheets decrease in thickness lat- 
erally and thin out toward the ventral margins of the shell. 
In several specimens showing extensive dissolution on the 
exterior shell surface away from the umbonal region and 


Figure 6 


Enlarged view of the inset area in Figure 5. m, microtube; o, 
organic sheet; ds, dissolved surface; dp, depositional surface. Unit 
of scale in microns. 


at the depositional surface of the umbonal region. Same specimen as in Figure 4D, E. G. Fibrous substance occurring 
from the openings of microtubes. UMUT RM 19110. H. Enlarged view of fibrous substance in Figure 4G. 
Depositional surface is toward the bottom of the figure in Figure 4A-E. The venter is toward the right in Figure 
4G, H. cl, crossed-lamellar layer; 0, organic sheet; pr, prismatic layer. Unit of scale in microns. 


Page 172 


manifest as a deeply dissolved pit, similar organic sheets 
were observed as irregular patches in the inner shell layer 
just beneath the deeply dissolved pit (Figure 5). Complete 
dissolution exposing the outer mantle epithelium was not 
observed in any specimen. Such organic sheets were not 
observed in most examined specimens not showing disso- 
lution in the umbonal region. 

Besides the organic sheets, numerous microtubes occur 
locally within the inner shell layer in the umbonal region 
(Figures 4-6). These microtubes are 10-30 wm in diameter 
and circular to elliptical in cross section (Figure 4A-D). 
The inner surface of the microtubes is covered by a thin 
prismatic wall (about 5-15 wm thick) which is clearly 
distinguished from the crossed-lamellar structure of the 
inner shell layer (Figure 4E). These microtubes open into 
depressions on the inner shell surface around the umbonal 
cavity (Figure 4F, G). They occur abundantly near the 
inner shell surface of the umbonal cavity in large specimens 
but are rare in small specimens. In addition, in one large 
specimen, these microtubes occur abundantly on the inner 
side of the inner shell layer but gradually decrease in 
number toward the outer and ventral sides. The microtubes 
occur in all specimens regardless of whether or not shell 
dissolution has occurred. A fibrous substance occasionally 
occurs within these tubes, which may be the remains of 
some soft tissue (Figure 4G, H). Numerous micro borings 
(1 wm in diameter) also occur within both the outer and 
inner shell layers of the etched area of living specimens. 
Such micro borings lack thin prismatic walls on their inner 
surface. These borings appear to be made by endolithic 
microorganisms (e.g., bacteria, fungi and algae [LILJE- 
DAHL, 1986]) and are clearly distinguished from micro- 
tubes. 

No periostracum-like organic sheets have been observed 
in large specimens of brackish to freshwater corbiculids 
such as Corbicula leana Prime, C. sandai Reinhardt, C. 
japonica Prime, all of which have extensive dissolution in 
their umbonal region (S. Isaji, unpublished data). 


DISCUSSION 


Judging from their mode of distribution within the shell, 
periostracum-like organic sheets in the inner shell layer 
of Geloina appear to play a role in retarding the rate of 
shell dissolution. Most mollusks can repair their shell. 
BEEDHAM (1965) stated that Anodonta secretes organic 
sheets on the outer mantle surface when the shell is dam- 
aged. WATABE (1983) also documented that internal or- 
ganic sheets are observable in the repaired shells of several 
bivalve genera. In the case of Geloina, no specimens were 
observed whose umbonal region was completely eroded. 
Therefore, the organic sheets in the inner shell layer of 
Geloina were not secreted as damage-repair sheets. The 
restricted distribution of the organic sheets in the inner 
shell layer suggests that they were deposited in response 
to deep dissolution on the shell surface. Therefore, they 


The Veliger, Vol. 36, No. 2 


appear to have secreted from the inside of the shell by the 
mantle epithelium before the dissolution reached the in- 
ternal shell surface. According to KaT (1985), Geloina 
suborbiculata (Pilsbry) has organic sheets (4-6 um in thick- 
ness) in the inner shell layer and no more than two organic 
sheets were observed to occur in the shell of examined 
specimens. The differences in information about the thick- 
ness and number of organic sheets presented by KaT (1985) 
and in this study may be due to both species differences 
and degrees of shell dissolution of the examined specimens. 

Similar organic sheets have been found in the bivalve 
shells of several different taxa. KAT (1985) reported that 
organic sheets occur within the shell of some marine and 
brackish-water bivalve species distributed among three su- 
perfamilies (Solenacea, Corbiculacea, and Myacea) and 
are ubiquitous among freshwater Unionacea (see also 
TOLSTIKOVA, 1974). Such organic sheets may have an im- 
portant role in retarding the rate of shell dissolution under 
the low pH conditions of their habitats (TAYLOR e¢ al., 
1969; TEVESzZ & CaRTER, 1980; KAT, 1982, 1983, 1985). 
Lewy & SAMTLEBEN (1979) also reported the presence of 
internal organic sheets in corbulid shells, which they in- 
terpreted as resisting both predation by boring gastropods 
and shell dissolution. KAT (1985) also reported the simi- 
larities of microstructural features of organic sheets exist- 
ing in four different superfamilies. He stated that “these 
convergences may have arisen through a similarity of re- 
sponses to similar selection pressures and to constraints 
on the number of ways such organic sheets can be con- 
structed.” 

In the case of the Unionacea, extensively eroded shells 
have more numerous organic sheets than the shells without 
appreciable umbonal dissolution (TEVESZ & CARTER, 1980; 
KaT, 1983). Extensive shell dissolution can take place 
without lethal effects in the Unionacea. TEVESZ & CARTER 
(1980) have suggested that unionids can deposit patches 
of adventitious organic sheets near their umbonal region 
as a safeguard against possible deep umbonal dissolution. 
According to these authors, these prophylactic organic sheets 
can be distinguished from damage-repair sheets by their 
lack of an underlying prismatic layer. It is uncertain, how- 
ever, what kind of factor causes the formation of these 
prophylactic organic sheets of unionid shells (KAT, 1983). 

In all Geloina specimens that have suffered extensive 
shell dissolution in the umbonal region, microtubes occur 
locally within the inner shell layer in association with 
internal organic sheets. This correlation suggests that the 
microtubes may somehow be related to the formation of 
internal organic sheets in the inner shell layer. For in- 
stance, the microtubes may have housed soft tissue, and 
the tissue may have a sensory function related to the de- 
tection of shell dissolution. This hypothesis could be tested 
in part by histochemical examination of the soft tissue 
found in the microtubes. 

Tiny canals (3-9 um in diameter) similar to those ob- 
served in Geloina shells are known to occur in the small 


S. Isaji, 1993 


freshwater corbiculids of the family Pisidiidae. These ca- 
nals in the shells of the Pisidiidae are called punctae (Rosso, 
1954; ROBERTSON & CONEY, 1979). These punctae tunnel 
through both inner and outer shell layers but not through 
the periostracum layer. They are distributed broadly on 
the shell disc even in prodissoconch larval shells. All of 
the punctae housed tube-shaped projections of the outer 
mantle tissue (Rosso, 1954; ROBERTSON & CONEY, 1979). 
ROBERTSON & CONEY (1979) speculated that the punctae 
of Musculium securis (Prime) have a special function for 
respiration and/or monitoring the moisture content. The 
function of these punctae is unknown. In their mode of 
distribution within the shells, the punctae of Pisidiidae 
differ from those of Gelozna. 

HINCH & GREEN (1988) suggested that dissolution of 
the unionid shell is not related to differences in ambient 
water chemistry. They argued that shell dissolution in 
unionids is primarily a physical process probably related 
to water turbulence. It is certain that shell dissolution is 
initiated by abrasion of the periostracum of the umbonal 
region. However, once the periostracum has worn away, 
shell dissolution seems to be accelerated by low pH of the 
ambient water. In mangrove swamps, shell dissolution in 
Geloina does not appear to be affected by a difference in 
the grain size of the sediment of the habitats. Therefore, 
acidification of water in the mangrove swamps is assumed 
to be a major source of shell dissolution in Geloia. In 
addition, low water turbulence within the mangrove 
swamps promotes the chemical process of shell dissolution. 
On the other hand, acidic water is common in normal 
brackish to freshwater environments. Most large-sized 
specimens of the Corbiculidae inhabiting such environ- 
ments possess an eroded umbo. However, no distinct in- 
ternal organic sheets have been observed in other corbicu- 
lid shells inhabiting brackish to freshwater environments, 
although shell dissolution in the umbonal region is lethal 
(KaT, 1982). In contrast, Geloina species can secrete in- 
ternal organic sheets that prevent extensive shell dissolu- 
tion when the inner shell layer is exposed to the ambient 
water through exfoliation of the periostracum.' These or- 
ganic sheets permit survival of Geloina in mangrove swamps, 
where chemical shell dissolution occurs more easily than 
in normal brackish to freshwater environments. 


ACKNOWLEDGMENTS 


I wish to thank Professor Itaru Hayami, Professor Ka- 
zushige Tanabe (University of Tokyo) and Dr. David K. 
Jacobs (American Museum of Natural History) for critical 
review of the manuscript and for valuable comments. I am 
also grateful to Drs. Katsumi Abe and Tatsuo Oji (Uni- 
versity of Tokyo) for many helpful suggestions during the 
course of this work. Thanks are also due to Research 
Institute of Tropical Agriculture, University of the Ryu- 
kyus for providing support during fieldwork on Iriomote 
Island. 


Page 173 


LITERATURE CITED 


BEEDHAM, G. E. 1965. Repair of the shell in species of Ano- 
donta. Proceedings of the Zoological Society of London 145: 
107-124. 

GriER, N. M. 1920. On the erosion and thickness of shells of 
the freshwater mussels. Nautilus 34:15-22. 

Hincu, S. G. & R. H. GREEN. 1988. Shell etching on clams 
from low-alkalinity Ontario lakes: a physical or chemical 
process? Canadian Journal of Fisheries and Aquatic Sciences 
45:2110-2113. 

KaT, P. W. 1982. Shell dissolution as a significant cause of 
mortality for Corbicula fluminea (Bivalvia: Corbiculidae) in- 
habiting acidic waters. Malacological Review 15:129-134. 

Kat, P. W. 1983. Conchiolin layers among the Unionidae and 
Margaritiferidae (Bivalvia): microstructural characteristics 
and taxonomic implications. Malacologia 24:298-311. 

Kat, P. W. 1985. Convergence in bivalve conchiolin layer 
microstructure. Malacological Review 18:97-106. 

Lewy, Z. & C. SAMTLEBEN. 1979. Functional morphology and 
palaeontological significance of the conchiolin layers in cor- 
bulid pelecypods. Lethaia 12:341-351. 

LILJEDAHL, L. 1986. Endolithic micro-organisms and silicifi- 
cation of a bivalve fauna from the Silurian of Gotland. Le- 
thaia 19:267-278. 

Morton, B. 1975. The diurnal rhythm and the feeding re- 
sponses of the Southeast Asian mangrove bivalve, Geloina 
proxima Prime 1864 (Bivalvia: Corbiculacea). Forma et 
Functio 8:405-418. 

Morton, B. 1976. The biology and functional morphology of 
the Southeast Asian mangrove bivalve, Polymesoda (Geloina) 
erosa (Solander, 1786) (Bivalvia: Corbiculidae). Canadian 
Journal of Zoology 54:482-500. 

Morton, B. 1983. Mangrove Bivalves. Pp. 77-138. In: W. D. 
Russell-Hunter (ed.), The Mollusca, 6, Ecology. Academic 
Press: New York. 

PRASHAD, B. 1932. The Lamellibranchia of the Siboga Ex- 
pedition, Systematic Part 2, Pelecypoda. Siboga-Expeditie 
53:1-353. Brill: Leiden. 

ROBERTSON, J. L. & C. C. Congy. 1979. Punctal canals in the 
shell of Musculium securis (Bivalvia: Pisidiidae). Malacolog- 
ical Review 12:37-40. 

Rosso, S. W. 1954. A study of shell structure and mantle 
epitheliuim of Musculium transversum (Say). Journal of the 
Washington Academy of Sciences 44:329-332. 

Taytor, J. D., J. M. KENNEDY & A. HALL. 1969. The shell 
structure and mineralogy of the Bivalvia. Introduction. Nu- 
culacea-Trigonacea. Bulletin of the British Museum (Nat- 
ural History) Zoology, Supplement 3:1-125. 

Taytor, J. D., J. M. KENNEDY & A. HALL. 1973. The shell 
structure and mineralogy of the Bivalvia. Lucinacea-Clav- 
agellacea, conclusions. Bulletin of the British Museum (Nat- 
ural History) Zoology 22, No. 9:253-294. 

TEvesz, M. J. S. & J. G. CARTER. 1980. Environmental re- 
lationships of shell form and structure of unionacean bi- 
valves. Pp. 295-322. In: D. C. Rhoads & R. A. Lutz (eds.), 
Skeletal Growth of Aquatic Organisms. Plenum Press: New 
York and London. 

TOLSTIKOVA, N. V. 1974. Microstructural characteristics of 
freshwater bivalves (Unionidae). Paleontological Journal 
8:55-60. (Translation of Paleontologicheskii Zhurnal, No. 
1:61-65.) 

WatTABE, N. 1983. Shell repair. Pp. 289-316. In: A. S. M. 
Saleuddin & K. M. Wilbur (eds.), The Mollusca, 4, Phys- 
iology, Part 1. Academic Press: New York. 


The Veliger 36(2):174-177 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A New Species of C'ypraea from Samoa in the 


C’. cribraria complex 


by 


C. M. BURGESS 


2502 Manoa Road, Honolulu, Hawaii 96822, USA 


Abstract. 


Cypraea taitae, the eighth member of the C. cribraria complex of cowries, is described as 


a new species on the basis of conchological and external anatomical features which differ from those in 
C. astaryt Schilder, 1971, a close conchological relative, and from all others in the C. cribraria species 
complex. Cypraea fallax Smith, 1880, and C. bernard: Richard, 1974, are not considered members of 


the C. cribraria species complex. 


Cypraea taitae Burgess, sp. nov. 
(Figures 1-4, 8, 10) 


Description: Shell: Cypraeiform, elongate-ovoid, mod- 
erately small, 10-17 mm, with produced extremities. La- 
bial callus prominent; slightly umbilicated. Anterior ex- 
tremity prominent and pointing upward in two of the five 
paratypes. Columellar teeth fine, sharply cut, confined to 
aperture. Labial teeth slightly coarser, produced to cross 
about one-third of the base. Aperture narrow, curved to- 
ward the columellar lip. Fossula vertical, prominently 
ribbed with six denticles but without a sulcus. Dorsum 
gold colored with discrete white spots; mantle line definite 
and discrete. Spire pure white but dorsal pigment may 
encroach. Discrete brown to black spots (0.3 x 0.7 mm) 
confined to the top of the labial callus and not appearing 
to ascend onto dorsum; spots not always visible on lateral 
margin of labial base. Columella with similar spots con- 
fined almost always to lateral margins of white base. 
Animal characters: Mantle brilliant dark carmine, thin, 
not obscuring dorsal pattern. Papillae fingerlike, blunt, 
arising from circular area of discrete black dots. Other 
papillae prominent, widely spaced, resembling three or 
four beads on a string, decreasing in size from their bases. 
Some papillae white, bearing several tufts arising from 
terminal bead, forming two vertical rows equally spaced 
along full length of mantle. Siphon carmine, finely fringed 
with short processes shaped exactly like interstices between 
them. Tentacles darker carmine, clubbed, with still darker 
tips. Foot of same color as mantle, studded, as is mantle, 
with discrete black spots; crawling surface pale orange. 


Habitat: Three live specimens were collected by the author 
in 1965, near Lepua Village, Pago Pago, Tutuila, Amer- 


ican Samoa, on the north side of the harbor on the reef 
flat; the cowries were under large coral blocks at a depth 
of 1-3 m at low tide near the drop-off into deep water. 
Additional specimens were collected from the same area 
by Bob Purtymun (personal communication, 1977) who 
also found subfossil shells in Pago Pago Harbor dredgings 
at Aua. In Western Samoa, Terry Kurth (personal com- 
munication, 1975) collected three pairs, each of one large 
and one small specimen, at 7.6 m in a current-swept gap 
in the reef under small coral slabs. 


Measurements: See Table 1. 


Type locality: The reef near the village of Lepua directly 
across Pago Pago Harbor from the city, Tutuila, American 
Samoa, 140°W, 19°6’S. 


Range: American Samoa (C. M. Burgess & R. Purtymun, 
personal communication, 1977); Western Samoa (T. Kurth, 
personal communication, 1983); Fiji (GERNOHORSKY, 1965, 
non C. gaskoini); New Hebrides (now Vanuatu) (SCHILDER 
& CERNOHORSKY, 1967; DEBANT 1969, non C. fischeri 
Vayssiére, 1910). 


Type depository: The holotype, length 16.2 mm, width 
9.4 mm, is deposited in the Bernice P. Bishop Museum, 
Honolulu, Hawaii, BPBM 9966. Paratypes ‘“‘a” and “b” 
(Figure 1) are in the Purtymun collection, 1200 Brickyard 
Way, No. 407, Point Richmond, California 94801; para- 
types ‘“‘c” and “‘e” (Figure 1) are in the Burgess collection, 
2502 Manoa Road, Honolulu, Hawaii 96822; paratype 
“d” is in the McKinsey collection, 95-016 Kipapa Drive, 
Miliolani, Hawaii 96789. 


Etymology: This species is named for my wife, Grace 
Tait Burgess, whose love and willingness to continue to 


C. M. Burgess, 1993 Page 175 


Explanation of Figures 1 to 10 


Figures 1-4. Dorsal, right and left lateral, and ventral views of the holotype of Cypraea taitae. BPBM 9960. 
Produced extremities are clearly illustrated. 16.2 x 9.4 mm. Photo by O. Schoenberg-Dole. x 1.25 


Figures 5-7. Dorsal, right lateral, and ventral views of the holotype of C. astaryz. 16.6 mm. Photos by E. Alison 
Kay. 1.25 

Figures 8, 9. Spire views of the holotype of C. taitae (Figure 8), and a homeotype of C. astaryi from the Tuamotu 
Archipelago (Figure 9). Pigmented spire clearly illustrated. Photos by O. Schoenberg-Dole. x 1.25 


Figure 10. Left lateral views of the five paratypes of C. taitae. a. length 17.0, width 9.8 mm; b. length 15.8, width 
8.8 mm; c. length 13.6, width 7.7 mm; d. length 10.7, width 5.7 mm; e. length 9.8, width 5.10 mm. Photos by O. 
Schoenberg-Dole. x 1.25 


Page 176 


Table 1 


Cypraea taitae. Measurements and ratios. 


The Veliger, Vol. 36, No. 2 


Catalogue 
Depository number Locality 

Bishop Museum BPBM 9966 Lepua, 

(Burgess 756-1) American Samoa 

holotype 
Purtymun 10003 Aua, 

paratype a American Samoa 
Purtymun 10002 Lepua, 

paratype b American Samoa 
Burgess 756-2 Lepua, 

paratype c American Samoa 
McKinsey FO16A4 Taema Bank, 

paratype d American Samoa 
Burgess 756-3 Asau, 

paratype e Western Samoa 
Average 


type and retype unfamiliar words and names over almost 
a lifetime built a debt that I can never repay. 


Comparisons: Cypraea taitae is the eighth member of the 
C. cribraria group, species of which are characterized by 
their orange to reddish dorsal pigmentation. Shells of C. 
taitae are easily separated from all others in the complex, 
and differ from those of C. cribraria Linnaeus, 1758, C. 
cribellum, Gaskoin 1849, and C. catholicorum Schilder & 
Schilder, 1938, by the presence of prominent discrete brown 
to black spots on the columellar and labial margins. Oc- 
casional small pigmented blotches or a few tiny light brown 
flecks may be present on the shells of each of these three 
species, but cannot be confused with the prominent spotting 
of C. taitae. The shells of C. gaskoini Reeve, 1846, differ 
from those of C. tattae in that they are globose; also, the 
marginal spots are smaller and in fully adult specimens 
may cover much of the dorsum of the shell. The shells of 
C. esontropia Duclos, 1833, are larger (14-34.7 mm) and 
more globose than those of C. taitae, the dark-banded 
embryonal structure is visible through the larger dorsal 
spots, and the teeth are much coarser than those in C. 
taitae. In C. cumingu Sowerby, 1832, the teeth are much 
finer and the terminal margin of the anterior lip is concave 
and sharper than in C. tattae. 

Conchologically, shells of Cypraea taitae are most like 
those of C. astaryi (Schilder, 1971) (Figures 5-7, 9) but 
they differ in several respects. The anterior extremity of 
C. taitae is produced to the point where it is actually 
directed upward and extends from the shell to a prominent 
degree, and to a greater degree in two of the five paratypes. 
The shallow umbilicus of C. taitae is pure white and is 
without pigment except for the slight encroachment of the 
dorsal pattern; the umbilicus of C. astary: is a narrow but 
deep, pigmented pit. The posterior extremity of C. taitae 


Length Width Height L/W L/H Labial ae 
(mm) (mm) (mm) ratio ratio teeth teeth 
16.2 9.4 7.1 1.72 2.28 16 22 
17.0 9.8 ES 1.73 DeDs 18 27 
15.8 8.8 6.9 1.79 2.29 17 23 
13.6 Vall 6 New 2.27 15 20 
10.7 Bu 5 1.88 2.14 16 19 

9.8 5.1 4.4 1.92 2.23 15 18 
13.85 ES 6.15 1.8 2.25 16.1 Pi) 


is prominent but not so prominent as is the anterior ex- 
tremity; the anterior extremity of C. astary: is barely visible 
and in most specimens blends smoothly with the curve of 
the dorsum, a difference clearly seen in lateral views of 
both cowries. The shells of C. tattae are slender; those of 
C. astaryi (in all 17 specimens studied) are plump and loaf- 
shaped. The dorsal spots of C. taitae are rarely (one of six 
of the type lot) rimmed with a barely visible darker pigment 
ring which is a prominent character of C. astary:. The teeth 
of both species are similar in number and appearance. In 
C. astaryi the fossula is grooved and grossly ridged; in C. 
taitae it is shallow and receding. The shells in both species 
have prominent marginal spotting but in C. astaryz it is 
more profuse and the spots are larger and often more 
heavily pigmented. Only the edges of the labial basilar 
spots of C. taitae are visible on the extreme lateral margins; 
the spots in C. astary: are prominent and cover a portion 
of the base. 

The mantle characters in Cypraea taitae are also very 
distinctive; indeed, it is the only member of the C. cribraria 
species complex that has tufted papillae. The mantle is 
also distinguished from that in C. astary: by the papillar 
arrangement and by the discrete black spots which stud it 
and the foot. Neither tufted papillae nor the spots are 
present on the mantle of C. astary: (see Busson’s photo- 
graph of the mantle of C. astaryi in BURGESS (1985:250). 


Discussion and History 


From 1965 to 1985, references to Cypraea astaryi, C. 
gaskoini, and C. fischeri have been utterly confused. In 1986 
André Lefait of Papeete, Tahiti, sent me a number of 
cowries from the Marquesas Islands and the Tuamotu 
Archipelago that did not fit any of the descriptions of shells 
in the C. cribraria species-complex. Comparison with the 


C. M. Burgess, 1993 


Page 177 


holotype of C. astary:, however, showed that they were 
conspecific with that species. Similarly, comparison of the 
type of C. fischeri with an array of shells in the C. cribraria 
species-complex showed that it was conspecific with C. 
gaskoini. These determinations left the shells described here 
as C. taitae without a name, a circumstance now rectified. 

There are also some previously published figures both 
of shells and animals of Cypraea taitae which were ascribed 
to other species. These references include those of 
CERNOHORSKY (1965:3, figs. 1-4) who cites the shells as 
C. gaskoini from Fiji; SCHILDER & CERNOHORSKY (1967: 
6, figs. 2, 3) who cites the shells as C. cumingu from the 
New Hebrides; DEBANT (1969:6, fig. 1a, b) who also refers 
his shells to C. cumingii from the New Hebrides; BURGESS 
(1977: 2, unnumbered text figures); and BURGEss (1985: 
250, unnumbered figure) who refers his illustrations and 
animal description to C. astaryz. BURGESS (1985) was not 
aware that his Samoan Cypraea species was specifically 
different from C. astary: and the illustrations of the dorsal 
and ventral views of what was then thought to represent 
that species are those of C. tattae; the photograph of the 
animal is, however, that of C. astaryz. 

Two additional species have been suggested as members 
of the Cypraea cribraria species-complex: C. fallax Smith, 
1880 (see LORENZ & BIRAGHI, 1986) (= Cribraria hada- 
nightae Trenberth, 1973) and C. bernard: Richard, 1974. 
Both conchological and mantle characters suggest that they 
are members of a group of Cypraea other than that of the 
C. cribraria species-complex. The shells of C. fallax re- 
ported from Denmark Beach, near Albany, Western Aus- 
tralia (BURGESS, 1985), superficially resemble those of C. 
cribraria, but the dorsal spotting is not depressed as in the 
shells of C. cribraria and others in the complex (the de- 
pression is formed by a lack of deposition of the dorsal 
pigment). The spots are more variable in size, the teeth 
on the columella are more produced, the fossula is of a 
different type (consisting of a very prominent and grossly 
ridged structure), the mantle obscures the dorsal pattern, 
and the thick conical papillae on the mantle differ from 
the slender, sometimes tufted, beaded papillae in the C. 
cribraria species-complex. The shells of C. bernard: Rich- 
ard, 1974, from Hitiaa, Tahiti similarly lack the depressed 
dorsal spotting in the C. cribraria species-complex; the spots 
are more variable in size, the labial and columellar teeth 
are much heavier than they are in shells of other species 
in the complex, and the mantle is yellow-brown with thick 
fingerlike papillae with blunt white tips. 


ACKNOWLEDGMENTS 


I am grateful to Dr. Georges Richard, Museum National 
d’Histoire Naturelle, Paris, for permitting me to examine 
the holotype of Cypraea bernardi; to Professor Dr. Rudolf 
Kilias, Museum ftir Naturkunde, Humboldt-Universitat, 
Berlin, for permitting me to examine the holotype of C. 
astaryt; to Bob Purtymun for providing the specimens of 


C. taitae from Samoa that serve as paratypes (a and b); 
and to Ray McKinsey for the loan of his paratype (d). I 
am most grateful for the indispensable guidance given by 
Dr. E. Alison Kay, Professor of Zoology at the University 
of Hawaii, not only in the formation of this presentation 
but also for her shared knowledge of the Cypraeidae over 
many years. It was Dr. Kay who borrowed the holotypes 
that were so vital in establishing a new species. And, sincere 
thanks to Olive Schoenberg-Dole for the sharp photo- 
graphs shown here as Figures 1-4, 8-10. 


LITERATURE CITED 


BurGEss, C. M. 1974. A new cowry of the Cribraria group. 
Hawaiian Shell News 22(6), New Series (174):1, 4. 

BurcEss, C. M. 1977. The “new” cowries. Hawaiian Shell 
News 25(12), New Series (216):1-6, 8. 

BurRGEss, C. M. 1985. Cowries of the World. Gordon Verhoef 
Seacomber Publications: Capetown, South Africa. xiv + 289 
PP- 

CERNOHORSKY, W. 1965. A new geographical record from Fiji. 
Hawaiian Shell News 13(11), New Series (69):3. 

DEBANT, P. 1969. Observations on Cribraria fisheri, Vayssiére 
1910. Hawaiian Shell News 17(10), New Series (118):6-7. 

Ductos, P. L. 1833. Jn: Guerin-Meneville. A description of 
Cypraea esontropia. Magasin de Zoologie 3rd year. 37 pp., 
pls. 19-37. 

GASKOIN, J. S. 1849. Description of seven new species of Mar- 
ginella and two of Cypraea. Proceedings of the Zoological 
Society of London 17:17-23. 

LINNAEUS, CARL VON. 1758. Systema naturae per regna tria 
naturae. Editia decima reformata. Stockholm, Vol. Regnum 
Animale. 824 pp. 

LORENZ, F., JR. & G. BIRAGHI. 1986. A taxonomical revision 
of West Australian Cribrarulae. La Conchiglia 18(204-205): 
24-26. 

REEVE, L. 1846. Description of two new species of Cypraea. 
Proceedings of the Zoological Society of London 14:23. 
RICHARD, C. 1974. Adusta (Cribraria) bernardi, sp. n. (Meso- 
gastropoda, Cypraeidae) des Iles de la Societe et les porce- 
laines des Polynesie Francaise. Bulletin de la Societe des 
Etudes Oceaniennes (Polynesie Orientale) 16(1):377-383. 

SCHILDER, F. A. 1971. Zur Kenntnis der Cypraeidae 14. Eine 
neue Cribrarula. Archiv fur Molluskenkunde 101(5/6):297- 
299. 

SCHILDER, F. A. & W. CERNOHORSKY. 1967. Rediscovery of 
Cribraria fischeri Vayssiére. Hawaiian Shell News 15(3), 
New Series (86):5-6. 

SCHILDER, F. A. & M. SCHILDER. 1938. Description of two 
new cowries. Proceedings of the Malacological Society of 
London 23(3):114-115. 

SMITH, E. A. 1880. Descriptions of two new species of shells. 
Annals and Magazine of Natural History, Ser. 5, 8:441- 
442. 

Sowerby, G. B., II. 1832. A catalogue of the Recent species 
of Cypraeidae. The Conchological Illustrations. London. 18 
pp., 180 figs., 37 pls. 

TRENBERTH, P. 1973. A new subspecies of the species Cribraria 
Linne, 1758. Cribraria haddnightae from southwestern Aus- 
tralia. Malacological Society of South Australia 17:1. 

VAYSSIERE, A. 1910. Nouvelle etude sur les coquilles de quelque 
Cypraea. Journal de Conchyliologie 58:301-311. 


The Veliger 36(2):178-184 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


How Does Strombina Reproduce? Evidence from ‘Two 


Venezuelan Species (Prosobranchia: Columbellidae) 


by 


ROBERTO CIPRIANI anp PABLO E. PENCHASZADEH 


Departamento de Estudios Ambientales e Instituto de Tecnologia y Ciencias Marinas (INTECMAR), 
Universidad Simon Bolivar, A.P. 89000, Caracas 1080, Venezuela 


Abstract. The objective of this paper is to describe the spawn and the reproductive strategy of 
Strombina francesae and S. pumilio. Spawn of both species consists of grayish-white and dome-shaped 
egg capsules that are laid as a compact mass on living adult shells of the same species. The egg capsules 
of S. francesae, obtained at the Archipiélago de Los Roques, have a closed oval escape aperture at their 
top. In each egg capsule, five eggs that measure 571 + 35 um (n = 22 eggs) in diameter develop into 
embryos. Even though hatching was not directly observed, the absence of a velum and the presence of 
well-developed structures in late embryos indicate that hatchlings emerge from the egg capsules as 
crawling juveniles. The egg capsules of different specimens of S. pumilio were obtained at Bahia de 
Mochima and Isla Caribe. In each egg capsule, 3 to 5 eggs develop into embryos. The egg diameter of 
one spawn from Isla Caribe was 616 + 48 um (n = 22 eggs). Juveniles hatching from one spawn found 
at Las Maritas crawled out from an oval escape aperture located at one side of the case wall. No evidence 
of nurse eggs was found in egg capsules of either species. The simple domed egg-capsule shape has 
been reported for other columbellids and also for other families of gastropods. According to the literature 


we have reviewed, the egg diameters herein reported are the largest in the Columbellidae. 


INTRODUCTION 


Only six living species of Strombina Morch, 1852, have 
been reported for the western Atlantic: the first two re- 
corded were Strombina pumilio (Reeve, 1859), from Cu- 
mana, eastern Venezuela, and Strombina francesae J. Gib- 
son-Smith, 7m J. Gibson-Smith & W. Gibson-Smith, 1974, 
from Cayo Francés, Archipiélago de Los Roques (VINK, 
1979; JUNG, 1986, 1989). By contrast, 32 species of Strom- 
bina and related genera inhabit the eastern Pacific. This 
remarkable diversity difference has been mainly explained 
by the massive and wide-spread extinction of mollusks that 
occurred in the Caribbean province from the middle Plio- 
cene to the Pleistocene (VERMEIJ, 1978; JUNG, 1989). Due 
to the scarcity of information on the life habits of these 
genera, biological studies on these Caribbean species would 
give new insights to paleontology and biogeography re- 
search. Only indirect evidence of larval development of 
Sincola and Bifurcium (JUNG, 1986, 1989), and a statement 
on direct development of S. pumilio (PENCHASZADEH, 1988), 
have been previously reported. There is, however, a large 
number of reports dealing with the spawning and larvae 
of other columbellids (e.g., PETIT & RuisBEc, 1929; 
THORSON, 1940; FRANC, 1941; Bacci, 1947; KNUDSEN, 
1950; NATARAJAN, 1957; Marcus & Marcus, 1962; AMIO, 


1963; SCHELTEMA & SCHELTEMA, 1963; SCHELTEMA, 1969; 
RAEIHLE, 1969; D’AsArRo, 1970; BANDEL, 1974; FLORES, 
1978). The following is the first description of the spawn 
of S. francesae and S. pumilio. 


MATERIALS anpD METHODS 


The identification of Strombina francesae (Figure 1A) and 
S. pumilio (Figure 1B) follows JUNG (1989). Spawns of 
Strombina spp. were deposited at the Museo de Ciencias 
Naturales de la Universidad Simon Bolivar (MCNUSB). 
Scientific names have been cited as in the original reports. 

Observations on the egg capsules of Strombina francesae 
were made on those attached to one specimen (MCNUSB- 
H266), obtained by Donald Shasky in March 1990 at 
Cayo Dos Mosquises (Figure 2A), southwest of Archi- 
pielago de Los Roques (11°48'26”N, 66°53'16”W). Infor- 
mation about the egg capsules of S. pumilio was obtained 
from one specimen (MCNUSB-H267) captured in Sep- 
tember 1985 at Las Maritas (Figure 2B), a sandy beach 
at Bahia de Mochima (10°24'11"”N, 64°20'00”W) and from 
the egg capsules attached to three specimens captured at 
Isla Caribe (Figure 2C), a small island located on the 
northern coast of the Peninsula de Araya (10°42’11"N, 
63°52'57"W): one of them was obtained in June 1991 


R. Cipriani & P. E. Penchaszadeh, 1993 


Figure 1 


A. Strombina francesae, from Dos Mosquises Sur. B. Strombina 
pumilio, from Isla Caribe. Scale bar: 5 mm. 


(MCNUSB-H144), another specimen was captured in 
September 1991 (MCNUSB-H217), and the final one was 
collected in March 1992 (MCNUSB-H253). 

Hatchlings of Strombina pumilio were obtained from the 
egg capsules attached to one specimen that was captured 
at Las Maritas, brought to the laboratory, and maintained 
in an aquarium with aerated seawater. 

Length, width, height, aperture length, and aperture 
width were measured in egg capsules from different spec- 


VENEZUELA 


Page 179 


imens. The minimum straight distance, perpendicular to 
the length, measured from the lower border of the escape 
aperture to the border of the egg capsule base, was used 
as an indicator of the relative position of the escape ap- 
erture. This variable was defined as the aperture position 
and is listed in Table 1. The egg diameter of both species 
was determined from fixed, uncleaved zygotes. Uncleaved 
eggs, individuals at the trocophore stage, and early and 
late embryos were all counted from different egg capsules 
of single spawns to indirectly ascertain the presence of 
nurse eggs. Shell length of hatchlings and late embryos 
was measured from the tip of the shell to the tip of the 
siphon canal. Shell width was the maximum width, per- 
pendicular to the length. Both measurements were ob- 
tained with the shell aperture facing down. The counting 
of the number of whorls follows JUNG (1986). Measure- 
ments were made using a Zeiss Stemi IV stereoscopic 
microscope. 

An electron microscope (Phillips T-SEM 505) was used 
to photograph adult protoconchs, juvenile shells, and egg 
capsules. This material was cleaned with filtered seawater 
and kept in a 70% ethanol solution before being coated 
with gold. SEM photographs of adult protoconchs and 
juvenile shells were compared to confirm the identity of 
hatchlings. 


RESULTS 
Strombina francesae 


The specimen of Strombina francesae was found buried 
about 2 cm deep in coarse sand, in a sandy area covered 


Figure 2 


The three sampling areas of Strombina spp. on the Venezuelan coast are shown as A, B, and C on the bottom map. 
These areas are shown enlarged on the top. The black arrows on each map indicate the sampling sites. A. Archipiélago 
de Los Roques National Park. Arrow: Dos Mosquises area. B. Bahia de Mochima. Arrow: Las Maritas Beach. 
C. Detail of the northern coast of the Peninsula de Araya. Arrow: Isla Caribe. 


Page 180 


Figure 3 


SEM pictures of an egg capsule of Strombina francesae from Dos 
Mosquises. The membrane of the escape aperture has been re- 
moved. A. Side view. B. Top view. Scale bar: 0.5 mm. 


by algal drift, at 0.8 m depth. It measured 17 mm in total 
length. 

Almost all the egg capsules were arranged in a compact 
mass covering most of the body whorl and the last three 
teleoconch whorls. They were grayish-white, translucent, 
and semispherical (Figure 3A, B; Table 1). Their surface 


The Veliger, Vol. 36, No. 2 


LEO LX, 5 
Figure 4 
SEM detail of the surface of the egg capsule of Strombina francesae 


from Dos Mosquises. The enclosed area is enlarged on the right 
side of the figure. Scale bar: 0.25 mm. 


had small, faint and sinuous grooves that resembled a 
“fingerprint” (Figure 4). Their basal wall was usually 
oval and slightly concave but it was irregularly shaped 
when the egg capsules were tightly attached to each other 
or when they were laid over other egg capsules. There was 
a thin and narrow ringed flange around the base of each 
egg capsule, the border of which was always irregularly 
broken. There was a suture on the egg capsule wall run- 
ning longitudinally from one side of the egg capsule to the 
other, dividing it into two almost equal halves. Near the 
center of the egg capsule, the suture borders separated 
from each other, forming an oval escape aperture, which 
was covered by a thin, almost smooth and opaque mem- 
brane. 

Uncleaved zygotes, trocophore stages, and early and late 
embryos were all found in different egg capsules of the sin- 
gle studied mass, suggesting that it was formed by more than 
one spawn (Table 2). Eggs measured 571 + 35 um (n = 
22 eggs) in diameter. No evidence of nurse eggs was found. 
Of the seven fixed egg capsules that contained well-de- 
veloped individuals, only 24 shells from late embryos were 
intact, having from 1.25 to 1.5 whorls and measuring 990 


Table 1 


Dimensions of the egg capsules of Strombina francesae and S. pumilio. Data obtained from 12 egg capsules of each species 
are given in millimeters (mm). The MCNUSB catalog number is under the scientific name. The information is presented 
as mean + standard deviation. 


Species Length Width 
Strombina francesae 
H266 2.4 + 0.3 Prin (072 
Strombina pumilio 
H267 2.4 + 0.2 2 iia 


Strombina pumilio 


H217 2.1 + 0.1 


Aperture Aperture Aperture 
Height length width position 
13) == 0M eg) (0S) 0.9 + 0.05 0.5 + 0.10 
1d) 1012 1.3 + 0.1 1.1 + 0.1 0.1 + 0.05 
1431013 1.3 + 0.1 1.0 + 0.2 0.2 + 0.14 


R. Cipriani & P. E. Penchaszadeh, 1993 


Figure 5 


SEM picture of a late embryo shell of Strombina francesae. Scale 
bar: 0.25 mm. 


+ 46 wm in length and 751 + 31 wm in width (Figure 5). 

Though juvenile hatching was not observed directly, late 
embryos removed from the egg capsules showed a well- 
developed foot, which had an oval, thin and transparent 
operculum on its posterior end. Both cephalic tentacles 
were well developed. On the left side of the embryos, a 
long siphon extended from the mantle. No remains of 
velum were observed on these juveniles, even though the 
velum was present in earlier embryos removed from other 


Figure 6 


Strombina pumilio (MCNUSB-H144) from Isla Caribe, with egg 
capsules attached to shell. Scale bar: 5 mm. 


Page 181 


Figure 7 


SEM pictures of Strombina pumilio egg capsule, from Las Mar- 
itas. The membrane of the escape aperture has been removed. 
A. Side view. B. Top view. Scale bar: 0.5 mm. 


egg capsules. These morphological characters indicate that 
embryos hatch as crawling juveniles. 


Strombina pumilio 


Adults were found buried or crawling on sandy patches 
near or among turtle and eel grass beds, in water between 
2 to 6 m deep. The observed specimens measured from 18 
to 21 mm in length. 

Spawns were found in a compact mass covering most 
of the body whorl, especially around the shell aperture 
and the last two or three teleoconch whorls (Figure 6). 
Those attached directly to shell were dome shaped and 
their base was flat; the other ones, laid over other egg 
capsules, were irregular at the base, which became concave 
(Table 1). A narrow, thin and irregular flange surrounded 
the egg-capsule base. At both sides of the egg capsule, a 
curved suture on the wall ran longitudinally from one side 
of the egg capsule to the border of the oval escape aperture. 
The aperture was formed by the separation of both suture 
borders and was covered by an opaque membrane, located 
on one side of the egg-capsule wall (Figure 7A, B). The 


Page 182 


Table 2 


Number of eggs, developing embryos, and juveniles of 
Strombina francesae and S. pumilio. Trocophore stages and 
early embryos are considered under the column headed 
Developing embryos/capsule. The MCNUSB catalogue 
number is under the scientific name. Data in parentheses 
correspond to the number of full egg capsules. 


Total 

num- Un- 

ber cleaved 

of egg eggs/ Developing Late 


cap- cap- embryos/  embryos/ 
Species sules  sule capsule capsule 
Strombina francesae 62 5 (5) 5 (46) 5 (7) 
H266 
Strombina pumilio 15 — 3-5 5 (1) 
H267 mode = 5 
(12) 
Strombina pumilio 18 _ 3-4 3-4 
H217 mode = 3. mode = 3 
(10) (3) 
Strombina pumilio AS) SG) 3-5 os 
H253 mode = 3 
(19) 
Strombina pumilio 25) — 4-5 — 
H144 mode = 5 
(20) 


surface of the wall and membrane was covered by nu- 
merous short and crossed grooves (Figure 8). 

Uncleaved zygotes from seven egg capsules found on one 
specimen from Isla Caribe (MCNUSB-H253) measured 
616 + 48 um in diameter (Table 2). Evidence of nurse 
eggs was not found. Furthermore, undeveloped eggs were 
not found on egg capsules containing developed embryos, 


SEM detail of the surface of the egg capsule of Strombina pumilio, 
from Las Maritas. The enclosed area is enlarged on the right 
side of the figure. Scale bar: 0.25 mm. 


The Veliger, Vol. 36, No. 2 


Figure 9 


SEM picture of a juvenile shell of Strombina pumilio hatched 
from a spawn collected at Las Maritas. Scale bar: 0.25 mm. 


and yolk remains were not found in all the egg cases 
analyzed. 

At hatching, juveniles from Las Maritas showed a well- 
developed foot and crawled out of the capsule through the 
escape aperture. A small, elongated, thin and translucent 
operculum was observed on the posterior end of the foot. 
Both cephalic tentacles were well formed. No remains of 
velum were observed on these juveniles or on late embryos 
removed from egg capsules attached to Isla Caribe speci- 
mens. A long siphon was also present. Well-preserved 
shells of 11 hatchlings from Las Maritas spawn showed 
from 1.25 to 1.5 whorls and measured 947 + 97 um in 
total length and 855 + 91 wm in maximum width (Figure 
wD), 


DISCUSSION 


Strombina pumilio and S. francesae do not seem to be the 
only species of this genus to use their own shells as a 
spawning substrate. Roundish egg capsules attached to 
shells of Strombina lanceolata (G. B. Sowerby, 1832) from 
the Galapagos Islands have been shown by JUNG (1989: 
60, fig. 82, pls. 19-21), and other eastern Pacific strom- 
binids seem to follow the same pattern (Dr. Beatrice Moor, 
unpublished observations). Laying egg capsules on the 
living shells of its own species seems to be also the most 
common behavior of the columbellid Mazatlania aciculata, 
which inhabits sandy beaches along the Venezuelan coast 
(PENCHASZADEH et al., 1983). 

The simple domed egg-capsule pattern has been re- 
ported for a number of families like Muricidae, Buccini- 
dae, Nassaridae, Mitridae, and Turridae (THORSON, 1940; 
BANDEL, 1974). Similar but smaller than Strombina egg 
capsules are those of Mitrella argus (Orbigny, 1842) and 
Mazatlania aciculata (BANDEL, 1974; PENCHASZADEH et al., 


R. Cipriani & P. E. Penchaszadeh, 1993 


Page 183 


1983). Egg capsules of other columbellids that have the 
same basic shape but are decorated with variable axial 
ribs and concentric ridges are those of Columbella merca- 
toria (Linné, 1758) and C. rustica (Linné, 1758), Anachis 
veleda (Duclos, 1846), A. pulchella (Blainville, 1829), M:- 
trella ocellata (Gmelin, 1791), and Pyrene rosacea Gould 
(THORSON, 1935; Bacct, 1947; Marcus & Marcus, 1962; 
BANDEL, 1974). Nevertheless, the most similar egg cap- 
sules to those described for Strombina spp. seem to be those 
reported by AMIO (1955) for Pyrene misera (G. B. Sowerby, 
1844), which seem to have a reticulated wall surface, as 
in S. pumilio, “but fibrous” according to the author, with 
their exit hole, located near the top of the case, as in S. 
francesae. The relative position of the escape aperture and 
the morphology of the wall surface are the major differ- 
ences between egg cases of both Strombina species. 

Of the 40 columbellid species reviewed, we found 16 in 
which juveniles hatch from the egg capsules as crawling 
snails. Columbella blanda and C. rustica have egg diameters 
clearly smaller than those reported herein for Strombina, 
160-180 and 280 um, respectively (THORSON, 1940; FRANC, 
1941; Baccl, 1947), and their embryos feed on nurse eggs 
to reach full development. An identical pattern of nurse- 
egg feeding seems to occur in Anachis avara, Columbella 
mercatoria, C. flava, Nitidella ocellata, and Pyrene misera, 
even though the egg diameter of Pyrene varies from 315 
to 320 um (PETIT & RISBEC, 1929; PERRY & SCHWENGEL, 
1955; Amio, 1955, 1963; RAEIHLE, 1969; BANDEL, 1974; 
FLoreEs, 1978). Although P. linschke: (Smith, 1879) have 
one of the largest uncleaved egg diameters reported in 
columbellids (390 um) (AMIo, 1957, 1963), the egg size 
of the Strombina species is almost twice as large, becoming 
the largest ever reported in this family. 

Anachis avara (Say, 1822), reported by FLoREs (1978), 
A. iontha, A. pulchella (Ravenel, 1861), Nitidella nitida 
(Lamarck, 1822), Pyrene linschkei, two unidentified species 
of Anachis (RAEIHLE, 1969; BANDEL, 1974), and two un- 
identified species of Columbella (LEBOUR, 1945; AMIO, 1963) 
show a lecithotrophic strategy with embryos undergoing 
intracapsular development, not feeding on nurse eggs, as 
in both Strombina species (AMIO, 1957, 1963; BANDEL, 
1974). 


ACKNOWLEDGMENTS 


The authors would like deeply to thank Donald Shasky 
for his valuable collaboration during his sampling trip to 
Los Roques in 1990. Special thanks go also to Dr. Peter 
Jung, Dr. Eugene Coan, Dr. Patricia Miloslavich, Dr. 
Beatrice Moor, and two anonymous reviewers for their 
help and for making valuable criticisms on this paper. We 
are grateful to Dr. Jack Gibson-Smith, the Fundacion 
Cientifica Los Roques, the Unidad de Fotografia of the 
Universidad Simon Bolivar, Dr. Walter Sage III], SEM 
technician Paulo Frias, Juan Carlos Urbina, Dr. Susan 
Bahar, Dr. Mary Gonzatti, and Lic. Maria Angelica Tal- 
amo. This research has been partially supported by a grant 


of the Decanato de Investigacion y Desarrollo of the Univ- 
ersidad Simon Bolivar. 


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Amio, M. 1963. A comparative embryology of marine gastro- 
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Bacci, G. 1947. Le capsule ovigere di Columbella rustica (L.) 
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BANDEL, K. 1974. Spawning and development of some Col- 
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D’Asaro, C. 1970. Egg capsules of some prosobranchs from 
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The Veliger 36(2):185-198 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A Review of the Genus Kaiparathina Laws, 1941 
(Mollusca: Gastropoda: Trochoidea) 


BRUCE A. MARSHALL 


Museum of New Zealand Te Papa Tongarewa, P.O. Box 467, Wellington, New Zealand 


Abstract. The genus Kaiparathina Laws, 1941, is referred to the trochid subfamily Margaritinae in 
anew tribe, Kaiparathinini. The type species of Kaiparathina, K. praecellens Laws, 1941 (Early Miocene, 
New Zealand) is illustrated, Calliotrochus navakaensis Ladd, 1982 (Pleistocene, Vanuatu) is referred to 
the genus, and the following new Recent species are described: K. boucheti and K. vaubani (New 
Caledonia), K. coriolis (northern Lord Howe Rise), K. fasciata (southern Norfolk Ridge), K. daedala 
(Réunion). Kazparathina senex sp. nov. is based on a specimen from the Late Paleocene-Early Eocene 


of the Chatham Islands, New Zealand. 


Kaiparathina species have an extremely distinctive radular morphology and are unique among ar- 
chaeogastropods in having large, clearly delineated zones of unknown function on each side between 
the epipodial fringe and the sole. They are evidently sponge-feeders. 


INTRODUCTION 


Kaiparathina Laws, 1941, was proposed for a distinctive 
gastropod (K. praecellens Laws, 1941) from the richly fos- 
siliferous Early Miocene beds at Pakaurangi Point, Kai- 
para Harbour, northern New Zealand. Although Laws 
(1941) did not specifically refer Kaiparathina to any family, 
the bestowed name and comparative remarks clearly in- 
dicate that he considered it to belong to the Janthinidae. 
BEU (1973) subsequently noted that the type species has 
a nacreous layer and thus referred it to Trochidae. The 
present contribution was initiated when I realized that 
Calliotrochus navakaensis Ladd, 1982, and some unde- 
scribed Recent species belong in Kaiparathina. Recent Kar- 
parathina species occur in the tropical and subtropical Indo- 
West Pacific on or near rocky substrata at 133-610 m 
depth (living specimens from rocky ground at 210-610 m). 


Abbreviations: AMS—Australian Museum, Sydney; 
AUG—Auckland University Geology Department; 
BMNH—tThe Natural History Museum, London; 
LACM—Los Angeles County Museum of Natural His- 
tory; MNHN—Museum National d’Histoire Naturelle, 
Paris; MNZ—Museum of New Zealand, Wellington; 
NMP—Natal Museum, Pietermaritzburg; NZGS—In- 
stitute of Geological and Nuclear Sciences, Lower Hutt; 
USNM—National Museum of Natural History, Wash- 
ington D.C. 


SYSTEMATIC TREATMENT 
Order Archaeogastropoda Thiele, 1925 
Suborder Vetigastropoda Salvini-Plawen, 1980 
Superfamily TROCHOIDEA Rafinesque, 1815 
Family TROCHIDAE Rafinesque, 1815 
Subfamily MARGARITINAE Stoliczka, 1868 
Tribe Kaiparathinini Marshall, new 


Distribution: Late Paleocene-Recent, tropical and sub- 
tropical southwest Pacific and Réunion. 


Diagnosis: Shell similar to those of Margaritinae, an- 
omphalous, with peripheral keel and sigmoidal collabra! 
growth lines on base, spirally sculptured. Snout fringed 
with papillate processes, prominent propodial horns, no 
cephalic lappets. Large, swollen, clearly delineated, sub- 
circular anterolateral structures on each side of foot be- 
tween epipodial fringe and sole. Ctenidium bipectinate, 
afferent membrane short. Central and lateral radular teeth 
strongly hooded and flanged, central tooth exceptionally 
large; shafts of all but innermost and outermost marginal 
teeth incompletely separated; innermost marginal not en- 
larged. 


Description: Shell conispiral, up to about 10 mm high, 
thin to rather thick, anomphalous, glossy, nacreous within, 


Page 186 


teleoconch frequently with supramedian and peripheral 
rows of spots and/or wavy axial lines. Protoconch smooth 
apart from few fine spiral threads. Teleoconch whorls all 
convex or becoming almost flat, periphery weakly or 
strongly angulate, base weakly convex or more or less flat; 
periphery with rounded spiral cord; all spire whorls or 
first 2 spire whorls spirally lirate; base with or without 
spiral lirae; collabral growth lines weakly sigmoidal on 
spire, more strongly sigmoidal on base. Aperture subcir- 
cular, peristome discontinuous. Operculum chitinous, mul- 
tispiral, thin, growing edge short. Animal with prominent 
papillate processes at broad snout edge. Large swollen, 
subcircular anterolateral structures on each side of foot 
between non-digitate epipodial fringe and sole; each an- 
terolateral structure bounded by low ridge, comprising 
crowded, minutely pustulose, hemispherical structures 
(histology and function unknown). Epipodial tentacles of 
moderate size, minutely and densely papillate, numbering 
3 on each side; no cephalic lappets, neck lobes simple; 
prominent propodial horns. Ctenidium large, bipectinate, 
free tip long and tapered, leaflets on right side thicker, 
afferent membrane short. Radular teeth in about 40 cross 
rows, central field evenly curved; central and lateral teeth 
stout, with angulate, strongly hooded cutting areas, shafts 
laterally flanged and grooved, faces thickened, central tooth 
relatively large; lateral teeth multiplying by progressive 
in-column morphological transformation of marginal teeth 
into a late stage of ontogenesis, smoothly enlarging out- 
wards, 4-9 pairs per cross row at maturity; no latero- 
marginal plates; marginal fields narrow, teeth numerous, 
morphologically grading rather smoothly into laterals, 
slender, tips rounded and finely serrate, outermost mar- 
ginal much broader than inner marginals, shafts of all but 
innermost and outermost teeth incompletely separated. Jaws 
present. 


Remarks: Although undoubtedly trochoidean, species of 
Kaiparathina cannot be satisfactorily grouped into any of 
the known families or subfamilies as defined by HICKMAN 
& McLEAN (1990). Among Trochoidea, the topographi- 
cally complex, strongly hooded, laterally interlocking teeth 
of the central radular field are most similar to those in 
adult Eucylinae, especially Calliotropini (HICKMAN & 
MCLEAN, 1990:figs. 43, 47), the radula differing princi- 
pally by having a relatively larger central tooth, and in- 
completely separated marginal teeth with broad comblike 
cutting areas. The ctenidium most closely resembles those 
in Eucyclinae, Margaritinae, and Tegulinae, which differ 
markedly from those of other trochid subfamilies (HICK- 
MAN & MCLEAN, 1990). This ctenidial type—fully bi- 
pectinate with a long free tip and a short afferent mem- 
brane—is characteristic of trochoideans with particularly 
long fossil records, and has been interpreted by HICKMAN 
& McLEAN (1990) as a plesiomorphy. Kaiparathina seems 
unlikely to be closely related to Eucyclinae, in which the 
shell sculpture is predominantly axial, especially on the 
early teleoconch whorls, while the heavy shells of the lit- 


The Veliger, Vol. 36, No. 2 


toral or shallow sublittoral Tegulinae are entirely dissim- 
ilar. Among the three subfamilies, shell morphology most 
closely approaches that of Margaritinae, in which spiral 
sculpture is also predominant, if not on all teleoconch 
whorls then usually on the earliest ones. Although prob- 
ably independently derived, some aspects of head-foot mor- 
phology approach those exhibited by Gaza superba (Dall, 
1881) (Margaritinae, Gazini) in which the edge of the 
oral shield is digitate, and the foot has anterolateral pro- 
jections. Gaza superba is, however, strongly dissimilar in 
size and in shell and adult radular morphology, and in 
other aspects of head-foot morphology (HICKMAN & 
McLEan, 1990). 

The central and lateral radular teeth of all known adult 
margaritines differ from those in Kazparathina by having 
strongly outwardly bowed shafts, broader and flatter shaft 
faces, and non-hooded cutting areas (HICKMAN & Mc- 
LEAN, 1990:figs. 50, 53). As shown by WAREN (1990), 
trochoidean radulae undergo often profound progressive 
morphological transformations during ontogenesis, and the 
radulae of most juvenile trochoideans (with the notable 
exception of calliostomatids) are at first essentially similar 
to each other. For this reason it is unnecessary to invoke 
progressive “horizontal” evolutionary transformations to 
derive divergent radular morphologies from one another. 
Since adult radulae of Kaiparathina species are not unlike 
those of juvenile trochoideans in general (WAREN, 1990), 
it would seem that somatic development of their radulae 
is retarded (paedomorphosis) relative to that in Margariti- 
nae, Eucyclinae, and Tegulinae. This contention is sup- 
ported by the relatively narrow marginal fields with rel- 
atively low numbers of incompletely separated teeth. 

Accordingly, and despite the differences in adult rad- 
ulae, I conclude that Kaiparathina and Margaritinae are 
related. While this group may well prove worthy of sub- 
familial status on the basis of additional data (e.g., ana- 
tomical and molecular), for the present I regard it as a 
clade within Margaritinae, for which the informal tribal 
name Kaiparathinini is introduced. 

Intestinal tracts of specimens of Kazparathina boucheti 
contain much fine, white matter of unknown origin to- 
gether with numerous minute, silicious sponge spicules, 
predominantly tetraxonic. That these spicules are the re- 
mains of prey rather than incidentally ingested components 
of detritus is suggested not only by their quantity but also 
by the large size and morphology of the central radular 
tooth, which seems to be ideally suited for prey penetration 
and slicing rather than for detrivory or deposit feeding. 
Sponge feeding is rare among Trochoidea and is known 
only in a few species of Calliostomatidae (summarized by 
MARSHALL, 1988) and in at least some of the Trochacli- 
didae (HAIN, 1990; HICKMAN & MCLEAN, 1990; personal 
observations). 

The anterolateral fields on the sides of the foot are a 
radical departure from the standard trochoidean plan and 
are clearly apomorphic (Figures 1-3, 5). Their function 
is unknown. 


B. A. Marshall, 1993 Page 187 


Explanation of Figures 1 to 5 


Figures 1-5. Kaiparathina boucheti Marshall, sp. nov. Critical-point dried animal (retracted, unfixed, ex alcohol), 
MUSORSTOM 4 sta. DW221. Figures 1-2. Head-foot, subject length 4.8 mm; note prominent propodial horns 
inclined to animal’s left in Figure 1. Figure 3. Detail of tip of right cephalic tentacle and ventral margin of right 
anterolateral structure. Figure 4. Detail of dorsal surface of right cephalic tentacle (right) and tentaculiform processes 
at snout edge. Figure 5. Detail of right anterolateral structure showing granulate surface. als, anterolateral structure; 
ct, cephalic tentacle; es, eyestalk; et, epipodial tentacle; fo, foot; op, operculum; sn, snout. Scales = 100 um. 


Page 188 The Veliger, Vol. 36, No. 2 


Explanation of Figures 6 to 17 


Figures 6-17. Kaiparathina species. 


Figures 6,9, 12. K. senex Marshall, sp. nov., holotype, Late Paleocene-Early Eocene, Pitt Island, Chatham Islands, 
w Zealand, shell height 3.90 mm. Detail width in Figure 9 = 1.60 mm, Figure 12 = 970 um. 


Figures 7, 10, 13, 15. K. praecellens Laws, 1941, Early Miocene, Pakaurangi Point, Kaipara Harbour, New 


B. A. Marshall, 1993 


Genus Kaiparathina Laws, 1941 


Kaiparathina Laws, 1941:145. Type species (by original des- 
ignation): Kaiparathina praecellens Laws, 1941; Early 
Miocene, Pakaurangi Point, Kaipara Harbour, New 
Zealand. 


Diagnosis and Description as for Kaiparathinini. 


Kaiparathina praecellens Laws, 1941 
(Figures 7, 10, 13, 15) 


Kaiparathina praecellens LAws, 1941:145, pl. 19, fig. 38; 
FLEMING, 1966:49; JONES, 1970:164; Bru, 1973:320, 
figs. 19, 20; BEU & MAXWELL, 1990:404. 


Type data: Holotype NZGS TM 1400: Pakaurangi Point, 
Kaipara Harbour, New Zealand; Otaian (Early Miocene). 


Other material examined: (7 specimens MNZ, 10 
NZGS). Tuffaceous siltstone, small bay ca. 1.6 km NW 
of Pakaurangi Point, Kaipara Harbour, New Zealand, 
map ref. Q8/262513 (f 9828), March 1979, B. A. Mar- 
shall and P. A. Maxwell; Otaian (Early Miocene). 


Distribution: Early Miocene (Otaian), Pakaurangi Point, 
Kaipara Harbour, northern New Zealand. 


Remarks: As noted by LAws (1941) some specimens retain 
traces of the original color pattern, which is evidently 
restricted to the last adult whorl; it comprises wavy axial 
lines that extend abapically from about midway between 
the suture and periphery and across the base. The lines 
are gently opisthocline on the spire, and so strongly opis- 
thocline as to be almost spiral on the base. A somewhat 
similar color pattern is exhibited by Kaiparathina nava- 
kaensis (Ladd, 1982) and K. vaubani sp. nov. (Figure 27). 
JONEs (1970) concluded that beds containing K. praecellens 
were deposited in a warm sea at up to about 250 m depth. 


Kaiparathina senex Marshall, sp. nov. 
(Figures 6, 9, 12) 


Description: Shell (holotype) 3.90 mm high, higher than 
broad, spire 1.5 as high as aperture, of moderate thick- 
ness, anomphalous. 

Protoconch 430 um wide, surface etched away. 

Teleoconch of 4.4 whorls. First 1.5 whorls evenly con- 
vex, subsequent whorls weakly convex, periphery angu- 
late, base more or less flat. First whorl with 5 rounded, 
closely spaced spiral cords, multiplying to 10 on subsequent 
whorls, peripheral spiral strongest, rounded, others broad 


Page 189 


and flattened with sublinear interspaces. Base with 15 
similar, rounded spiral cords with interspaces about as 
wide as each spiral. Collabral growth lines prosocline on 
spire, sigmoidal on base. Aperture subquadrate, outer lip 
thin, inner lip thick. 


Type data: Holotypes NZGS TM 7301, GS 12159 (CH/ 
£471), Coarse Red Bluff Tuff on large wave-cut platform 
and in low outcrops at base of cliff below Pliocene section 
on cliff due north of The Bluff homestead (grid ref. NZMS 
260/234712), Pitt Island, Chatham Islands, New Zealand, 
Jan. 1977, A. G. Beu, P. A. Maxwell and H. J. Campbell: 
Late Teurian-Early Waipawan (Late Paleocene-Early 
Eocene). 


Distribution: Late Paleocene-Early Eocene (Late Teu- 
rian-Early Waipawan), Pitt Island, Chatham Islands, New 
Zealand. 


Remarks: Kaiparathina senex differs from all other species 
of Kaiparathina by having a larger protoconch, and more 
numerous and persistant spiral cords on the spire. Kai- 
parathina daedala sp. nov. has a similar number of weaker 
spiral cords on the base. 

According to BEU & MAXWELL (1990:88) the Red Bluff 
Tuff faunules inhabited a hard substratum on the summits 
or flanks of volcanic sea-mounts in an oceanic environment, 
probably at outer shelf or bathyal depths. 


Etymology: Old (Latin). 


Kaiparathina navakaensis (Ladd, 1982) 
(Figures 8, 11, 14, 27; Table 1) 
Calhiotrochus navakaensis LADD, 1982:24, pl. 34, figs. 9-11. 


Type data: Holotype, USNM 214405: United States Geo- 
logical Survey loc. 24198, Navaka River, Santo, Vanuatu; 
Pleistocene. 


Other material examined: 1 topotype USNM. 
Distribution: Pleistocene, Santo, Vanuatu. 


Remarks: Although originally referred to the genus Cal- 
liotrochus Fischer, 1879 (type species Turbo phasianellus 
Deshayes, 1863), Ladd’s species clearly belongs in Kar- 
parathina. The type species of Calliotrochus (DESHAYES, 
1863:pl. 36, figs. 13, 14; WENZ, 1938:fig. 620) differs 
markedly in shell facies and the genus apparently belongs 
in subfamily Trochinae, tribe Gibbulini (HICKMAN & 
MCLEAN, 1990). From the Recent species described here- 


Zealand, NZGS TM 7303. Figure 7. Shell height 2.30 mm. Detail width in Figure 10 = 900 um, Figure 13 = 


470 wm, Figure 15 shell width = 3.20 mm. 


Figures 8, 11, 14. K. navakaensis Ladd, 1982, Pleistocene, Santo, Vanuatu, USNM 459658, shell height 2.05 mm. 


Detail width Figure 11 = 950 um, Figure 14 = 480 um. 


Figures 16, 17. K. sp. cf. navakaensis Ladd, 1982, MUSORSTOM 6 sta. DW410, off Lifou, Loyalty Islands, 490 
m, MNHN, shell height 5.00 mm. Detail width in Figure 16 = 1.30 mm. 


Page 190 The Veliger, Vol. 36, No. 2 


Explanation of Figures 18 to 30 


Figures 18-30. Kaiparathina species. 


Figures 18, 21, 24. K. boucheti Marshall, sp. nov., holotype, BIOCAL sta. DW46, off southern New Caledonia, 
570-610 m, shell height 5.45 mm. Detail width in Figure 21 = 1.60 mm, Figure 24 = 530 um. 


Figures 19, 22, 25. K. vaubani Marshall, sp. nov., holotype, MUSORSTOM 4 sta. DW164, off northern New 
Caledonia, 255 m, shell height 3.70 mm. Detail width in Figure 22 = 1.00 mm, Figure 25 = 500 um. 


Figures 20, 23, 26, 28. K. coriolis Marshall, sp. nov., holotype, MUSORSTOM 5 sta. 309, Nova Bank, northern 
Lord Howe Rise, 340 m, shell height 10.1 mm. Detail width in Figure 23 = 1.70 mm, Figure 26 = 500 um. 


B. A. Marshall, 1993 


Page 191 


Table 1 


Kaiparathina navakaensis and K. sp. cf. navakaensis. Shell 
measurements (mm) and countings. 


Height/ Teleoconch 


Height Diameter diameter whorls Material 
5.00 4.90 1.02 4.60 DW410 
4.90 4.40 1.11 4.75 DW410 
3.90 3.25 1.20 4.60 Holotype 
2295 Dol 5) 1.07 3.70 DW08 
2.05 17/5) SH 3.50 Paratype 


in, the holotype of K. navakaensis is distinguished by its 
very thick shell, the weakly convex 2nd—4th teleoconch 
whorls, and the color pattern of dark, strongly opisthocline 
bands that are continuous across the spire and base. A 
topotype (Figures 8, 11, 14) resembles the holotype in 
shell thickness and sculpture, but differs by having a small- 
er protoconch (width 330 um instead of 370 um) and less 
markedly flattened teleoconch whorls. The specific status 
of this topotype cannot be resolved with such limited ma- 
terial, and it is only tentatively interpreted as K. nava- 
kaensis. 

Kaiparathina navakaensis may still be living off Vanuatu, 
and perhaps off the Loyalty Islands as well (see below). 


Kaiparathina sp. cf. navakaensis (Ladd, 1982) 
(Figures 16, 17; Table 1) 


Material examined: (3 specimens MNHN): BIOCAL 
sta. DW08, 20°34’S, 166°54’E, off Lifou, Loyalty Is., 
dead, 435 m, n.o. Jean-Charcot (1); MUSORSTOM 6 sta. 
DW410, 20°38’S, 167°07’E, off Lifou, dead, 490 m, n.o. 
Alis (2). 


Remarks: Three specimens dredged off Lifou, Loyalty 
Islands closely resemble the holotype of Kaiparathina na- 
vakaensis (Figure 27) in shell shape, sculpture, and thick- 
ness. They differ primarily by having slightly broader 
protoconchs (width 400 wm instead of 370 wm holotype 
and 330 um in topotype). Although all three are bleached 
and etched to some extent, the late teleoconch whorls of 
the two shells from station DW410 have a pale, dull, 
pinkish flush, and one has darker peripheral blotches. Ad- 
ditional, better preserved material from both Vanuatu and 
the Loyalty Islands will be required to ascertain the specific 
status of this form. 

Kaiparathina sp. cf. navakaensis and K. boucheti oc- 
curred together as shells at station DW0O8. 


Table 2 


Kaiparathina boucheti Marshall, sp. nov. Shell measure- 
ments (mm) and countings. 


Teleo- 
Height/ conch 
Height Diameter diameter whorls 


6.30 6.10 1.03 4.60 
5.90 5.40 1.09 4.80 
5.45 4.75 Neils) 4.50 
4.85 4.20 1.15 4.30 
4.65 4.05 1.15 4.30 
4.10 S)59)5) EIS) 4.10 


Material 


Paratype DW221 
Paratype DW221 
Holotype DW46 
Paratype DW46 
Paratype DW46 
Paratype DW46 


Kaiparathina boucheti Marshall, sp. nov. 
(Figures 1-5, 18, 21, 24, 39-44; Table 2) 


Description: Shell up to 6.30 mm high, slightly higher 
than broad, spire about as high as aperture, thin, trans- 
lucent, glossy, anomphalous. Protoconch reddish brown. 
Start of 1st teleoconch whorl reddish brown, rapidly fad- 
ing, uniformly nacreous through colorless outer shell layer 
after 1st 0.5-0.75 whorl. 

Protoconch 400-420 um wide, with 4 fine, crisp, widely 
spaced spiral threads. 

Teleoconch of up to 4.8 convex whorls, periphery weak- 
ly angulate, base gently rounded. First 2 whorls with crisp 
spiral threads that multiply by intercalation, spirals absent 
from adapical quarter, abapical (peripheral) threads per- 
sisting throughout, others weakening and vanishing on 
third whorl; spiral threads numbering 3 or 4 at start of 
1st whorl, multiplying to 6-8, narrow with broader in- 
terspaces on 1st whorl, after which broader with consid- 
erably narrower interspaces; abapical spiral gradually en- 
larging to form rounded peripheral spiral cord. Base with 
or without 1 or 2 spiral threads close beside peripheral 
spiral and columella; obscure spiral lines throughout. Ap- 
erture subcircular, outer lip thin, inner lip thick, parietal 
glaze very thin. Collabral growth lines prosocline on spire, 
sigmoidal on base. 

Animal (Figures 1-5) milky white. Snout tip broadly 
expanded, with prominent papillate processes. Cephalic 
tentacles large, dorsoventrally flattened, tapered, minutely 
and densely papillate, large eyes at tips of swollen outer 
basal eyestalks; neck lobes thin, not digitate, right consid- 
erably larger than left; epipodial tentacles of moderate size, 
minutely and densely papillate, 3 on each side; no cephalic 
lappets; large, swollen, clearly demarcated anterolateral 
structures between epipodial fringe and sole; foot large, 


Figures 27-30. Photographs of uncoated shells to show color patterns. Figure 27. K. navakaensis, Ladd, 1982, 
holotype, shell height 3.90 mm. Figure 28. K. coriolis Marshall, sp. nov., holotype, shell height 10.1 mm. Figure 
29. K. fasciata Marshall, sp. nov., holotype, shell height 3.35 mm. Figure 30. K. daedala Marshall, sp. nov., 


paratype (MNHN), shell height 4.05 mm. 


Page 192 


The Veliger, Vol. 36, No. 2 


Explanation of Figures 31 to 38 


Figures 31-38. Kaiparathina species. 


Figures 31, 34, 37. Kaiparathina fasciata Marshall, sp. nov., holotype, Wanganella Bank, southern Norfolk Ridge, 
133 m, shell height 3.35 mm. Detail width in Figure 34 = 1.00 mm, Figure 37 = 460 um. 

Figures 32, 33, 35, 36, 38. Kaiparathina daedala Marshall, sp. nov. Figures 32, 35, 38. Holotype, off Réunion, 
210-227 m, shell height 4.65 mm. Detail width in Figure 35 = 1.40 mm, Figure 38 = 470 um. Figures 33, 36. 
Paratype (MNHN), off Reunion, 280-340 m, shell height 4.05 mm, width 3.80 mm. 


elongate, with prominent anterior horns, posteriorly ta- 
pered. Operculum rather thin, chitinous, multispiral, 
growing edge short. 

Radula (Figures 39-44) with the formula 00 + 6 + 1 
+ 6 + 00. Central tooth large, very stoutly built, about 
as long as broad; cutting area narrowly angulate, strongly 
hooked, laterally flanged, edges finely serrate; terminal 
cusp large, slender; shaft face strongly thickened, back 
concave; base laterally flanged to interlock with lateral 
teeth. Lateral teeth progressively multiplying to 6 pairs by 
in-column transformation of marginals, longer than broad, 
elongating outwards, stout; cutting areas laterally flanged, 
narrowly tapered, finely serrate, terminal cusp large; shaft 
face strongly thickened, outer edge modestly flanged and 


inner edge very strongly flanged to interlock with adjacent 
teeth. Marginal teeth numerous; outermost tooth broad 
and laminar, inner teeth slender, tips blunt, finely serrate, 
shafts of all but innermost and outermost teeth incom- 
pletely separated. 

Jaw plates like those in Kaiparathina coriolis and K. 
daedala (see below). 


Type material: Holotype MNHN, and 4 paratypes (3 
MNHN, 1 MNZ): BIOCAL sta. DW46, 22°53’S, 
167°17'E, off S New Caledonia, alive, 570-610 m, n.o. 
Jean-Charcot. Paratypes (39): MUSORSTOM 4 sta. DW 
151, 19°07'S, 163°22'E, dead, 200 m, n.o. Vauban (1 
MNHN); BIOCAL sta. DW08, 20°54’S, 166°54’E, dead, 


B. A. Marshall, 1993 Page 193 


yr 


Explanation of Figures 39 to 44 


Figures 39-44. Kaiparathina boucheti Marshall, sp. nov., radulae. Figure 39. Entire width of radula from juvenile 
paratype, shell height 2.60 mm, showing 3 pairs of lateral teeth, MUSORSTOM 4 sta. DW221 (MNHN). Figure 
40. Part width of radula from adult paratype, shell height 3.65 mm, showing 6 pairs of lateral teeth, MUSORSTOM 
4 sta. DW221 (MNHN). Figures 41, 42, 44. Radula ex holotype. Figures 41, 42. Details of central and lateral 
teeth; note laterally flanged cutting areas, massive central tooth, and strongly laterally flanged shafts of lateral teeth. 
Figure 43. Bank of marginal teeth (lacking outermost tooth at right) from radula illustrated in Figure 44. Figure 
44. Tips of inner marginal teeth. Scales Figures 39-43 = 100 um, Figure 44 = 25 um. 


Page 194 The Veliger, Vol. 36, No. 2 


Explanation of Figures 45 to 50 


Figures 45, 46. Kaiparathina vaubani Marshall, sp. nov., holotype radula. Figure 45. Entire width. Figure 46. 
Detail of central (right) and lateral teeth. 


Figures 47-50. Kaiparathina coriolis Marshall, sp. nov., holotype radula. Figure 47. Entire width. Figure 48. Detail 
of central and lateral teeth. Figure 49. Detail of outermost lateral (right) and marginal teeth; note broad outermost 
marginal at lower left and incomplete separation of shafts of teeth above it. Figure 50. Side view of isolated column 
of central teeth showing the huge cutting area and short basal plate with interlocking lateral flanges and strong 
median boss. Scales = 100 pm. 


B. A. Marshall, 1993 


435 m, n.o. Jean-Charcot (8 MNHN); BIOCAL sta. DW 
83, 20°35'S, 166°54’E, dead, 460 m, n.o. Jean-Charcot (1 
MNHN); BIOGEOCAL sta. DW307, 20°35’'S, 166°55’E, 
dead, 470-480 m, n.o. Coriolis (1 MNHN); BIOCAL sta. 
KG 06, 20°36’'S, 166°53’E, dead, 735 m, n.o. Jean-Charcot 
(1 MNHN); MUSORSTOM 4 sta. DW225, 22°52’S, 
167°23'E, dead, 590-600 m, n.o. Vauban (1 MNHN); 
BIOCAL sta. CP 40, 22°55’S, 167°24'E, dead, 650 m, n.o. 
Jean-Charcot (1 MNHN); MUSORSTOM 4 sta. DW222, 
22°56'S, 167°33'E, alive, 410-440 m, n.o. Vauban (2 
MNHN); MUSORSTOM 4 sta. DW221, 22°59'S, 
167°37’'E, alive, 535-650 m, n.o. Vauban (25: 1 AMS, 1 
BMNH, 19 MNHN, 2 MNZ, 1 NMP, 1 USNM); SMIB 
4 sta. DW61, 23°00'S, 167°22'E, alive, 520-550 m, n.o. 
Alis (1 MNHN); BIOCAL sta. DW56, 23°35'S, 167°12’E, 
dead, 695-705 m, n.o. Jean-Charcot (1 MNHN). 


Distribution: Off northern and southern New Caledonia 
and northern Norfolk Ridge, 200-735 m, living at 410- 
610 m. 


Remarks: Kaiparathina boucheti differs from K. praecel- 
lans and K. navakaensis by having a thinner shell, a larger 
protoconch, and more strongly convex teleoconch whorls. 
Kaiparathina boucheti differs further by being more 
strongly and extensively sculptured on the early teleoconch 
whorls, by constantly lacking a color pattern, and by being 
larger relative to the number of whorls (Tables 1, 2). 


Etymology: Named after Philippe Bouchet (MNHN). 


Kaiparathina vaubani Marshall, sp. nov. 
(Figures 19, 22, 25, 45, 46; Table 3) 


Description: Shell up to 4.5 mm high, higher than broad, 
spire about as high as aperture, stout, glossy, anomphalous. 
Protoconch pinkish to blackish brown. First whorl choc- 
olate on adapical half, or 1st half whorl with pinkish 
subsutural zone, elsewhere translucent white. Subsequent 
whorls translucent white, internal nacreous layer showing 
through thin outer shell layers, with or without narrow, 
dull pink, opisthocline axial bands on 3rd whorl only, or 
on 3rd and subsequent whorls, including base. Inner lip 
white. 

Protoconch 330 um wide, with 3 fine, crisp spiral threads, 
otherwise smooth. 

Teleoconch of up to 4.75 convex whorls, periphery 
broadly rounded at maturity, weakly angulate before, base 
weakly convex. Peripheral keel narrow, rounded, adapical 
margin shelved and exposed on spire. First 2 spire whorls 
with 3 similar, narrow, rounded spiral threads on abapical 
half, their adapical margins sharply shelved, becoming 
obsolete at end of 2nd whorl. Subsequent whorls smooth 
apart from obscure spiral and collabral growth lines. Base 
with a spiral thread beside inner lip. Collabral growth 
lines prosocline, very weakly sigmoidal on spire, more 
deeply sigmoidal on base. Aperture subcircular, peristome 


Page 195 


Table 3 


Kaiparathina vaubani Marshall, sp. nov. Shell measure- 
ments (mm) and countings. 


Teleo- 
Height/ conch 


Height Diameter diameter whorls Material 


4.50 3295 1.14 4.75 Paratype CC175 
4.00 3.60 1.11 4.25 Paratype CC175 
3.85 3.50 1.10 4.20 Paratype DW38 
3.70 3.30 1.12 4.25 Holotype DW164 
2.60 2.45 1.06 3.20 Paratype DW38 


discontinuous; outer lip thin at rim, thicker and simple 
within; inner lip thick, parietal gaze very thin. 

Animal white, as in Kaiparathina boucheti but with 
longer, more narrowly tapered epipodial tentacles. Oper- 
culum as in K. boucheti. Jaw as in K. coriolis and K. 
daedala. 

Radula (Figures 45, 46) similar to that of Kaiparathina 
boucheti but with 4 lateral teeth, a much longer terminal 
cusp on central tooth, and sharper cusps on lateral teeth. 


Type data: Holotype MNHN: MUSORSTOM 4 sta. 
DW164, 18°33’S, 163°13’E, off d’Entrecasteux Reefs, N 
New Caledonia, alive, 255 m, n.o. Vawban. Paratypes (2): 
MUSORSTOM 4 sta. CC 175, 18°59'S, 163°17’E, off 
Grande Récif de Cook, N New Caledonia, dead, 355 m, 
n.o. Vauban (1 MNHN, 1 MNZ). 


Other material examined: (2 specimens MNHN): BIO- 
CAL sta. DW38, 23°00’S, 167°15’E, off Grand Recif du 
Sud, S New Caledonia, dead, 360 m, n.o. Jean-Charcot. 


Distribution: Northern and southern New Caledonia, 255- 
360 m, living at 255 m. 


Remarks: Kaiparathina vaubani differs from K. navakaen- 
sis and K. sp. cf. navakaensis by having a substantially 
thinner shell, slightly but distinctly stronger sculpture on 
the first teleoconch whorl, and more strongly convex te- 
leoconch whorls. Some specimens, including the holotype, 
resemble the holotype of K. navakaensis in color pattern, 
but the color bands in K. vaubani are narrower. It differs 
from K. boucheti by having a thicker shell, a smaller 
protoconch, by usually having axial color bands, and in 
details of radular morphology. 


Etymology: Named after n.o. Vauban, with which the type 
material was obtained. 
Kaiparathina coriolis Marshall, sp. nov. 
(Figures 20, 23, 26, 28, 47-50, 55, 56; Table 4) 


Description: Shell up to 10.1 mm high, slightly higher 
than broad, spire 0.74 (subadult) to 1.20 as high as 
aperture, stout, glossy, a narrow crescentic umbilical chink 


Page 196 


Table 4 


Kaiparathina coriolis Marshall, sp. nov. Shell measure- 
ments (mm) and countings. 


Height/ Teleoconch 


Height Diameter diameter whorls Material 
10.1 9.40 1.07 5.50 Holotype 
9.60 8.80 1.09 5.50 Paratype 
8.20 8.10 1.01 5.10 Paratype 


at maturity. Protoconch white. Teleoconch buff to pale 
pinkish buff, supramedian spiral on 1st 3 whorls and ex- 
posed part of peripheral keel on 1st 3.5 whorls alternately 
spotted white and reddish brown. Inner lip and base close 
beside it white, interior nacreous. 

Protoconch 400 um wide, 2 fine crisp spiral threads, 
otherwise essentially smooth. 

Teleoconch of up to 5.5 strongly convex whorls; pe- 
riphery evenly rounded at maturity, weakly angulate be- 
fore; base weakly convex. Peripheral keel rounded, almost 
entirely exposed on spire, becoming obsolete late on 5th 
whorl. Early whorls with rounded supramedian and su- 
prasutural spiral threads, the latter close beside peripheral 
keel. Supramedian spiral becoming obsolete late on 3rd 
whorl, narrow at first, gradually widening, bounded by 
grooves; adapical groove narrow throughout; abapical 
groove as broad as thread on 1st whorl, then progressively 
infilled by widening spiral thread. Suprasutural spiral 
bounded adapically by fine groove, becoming obsolete late 
on 2nd whorl. Elsewhere smooth apart from fine collabral 
growth lines, prosocline and shallowly sigmoidal on spire, 
more deeply sigmoidal on base. Aperture subcircular; outer 
lip thin at rim, thicker and simple within; inner lip thick, 
parietal glaze thin. 

Animal creamy white. Head broad, dorsoventrally flat- 
tened. Snout tip concave in front, fringed with prominent, 
finely and densely papillate projections. Cephalic tentacles 
tapered, dorsoventrally flattened, minutely and densely pa- 
pillate, well-developed eyes in prominent eyestalks at outer 
bases. Neck lobe on right considerably longer than broad, 
thin, extending from base of eyestalk, none on left. Epi- 
podial fringe prominent, 1 tapered epipodial tentacle on 
either side, 1 or 2 smaller tentacles on each side of opercular 
lobe. Anterolateral fields very large, clearly delineated. 
Foot longer than broad, anteriorly indented between prom- 
inent, tapered lateral horns. Operculum thin, chitinous, 
multispiral. 

Jaws (Figures 55, 56) thin, subrectangular with round- 
ed corners, elements minute. 

Radula (Figures 47-50) with the formula 00 + 9 + 1 
+ 9 + 00, 40 cross rows, teeth longer than broad. Central 
tooth relatively large, stout; cutting area large, laterally 
flanged, narrowly angulate, curved, sharply serrate; shaft 
face strongly thickened, shaft back concave; base flanged 
and grooved to interlock with laterals. Lateral teeth con- 


The Veliger, Vol. 36, No. 2 


siderably narrower than central; cutting areas narrowly 
angulate, outer edges laterally flanged and sharply serrate; 
shaft faces thickened, basal edges flanged and grooved to 
interlock with adjacent teeth. Marginal teeth slender, cut- 
ting areas rounded, leading edges finely serrate, shafts of 
all but innermost and outermost teeth incompletely sep- 
arated, outermost few pairs with very broad laminar shafts 
and smooth tips; innermost tooth morphologically inter- 
mediate between inner laterals and outer marginals. 


Type material: Holotype and paratype MNHN, paratype 
MNZ: MUSORSTOM 5 sta. 309, 22°10’S, 159°23’E, 
Nova Bank, alive, 340 m, n.o. Coriolis. 


Distribution: Nova Bank, northern Lord Howe Rise, 
340 m. 


Remarks: Kazparathina coriolis differs from other species 
of Kaiparathina by attaining much larger size, and by de- 
tails of teleoconch microsculpture, color, and color pattern. 
It differs further from K. boucheti and K. vaubani by 
having more numerous lateral teeth and by details of tooth 
morphology, particularly the presence of a relatively much 
smaller terminal cusp on the central tooth. 


Etymology: After n.o. Coriolis. 


Kaiparathina fasciata Marshall, sp. nov. 
(Figures 29, 31, 34, 37) 


Description: Shell (holotype) 3.35 mm high, slightly high- 
er than broad, spire evenly conical, 1.05 height of ap- 
erture, anomphalous, thin, translucent, glossy, nacreous 
through thin outer shell layer. Purplish brown beside su- 
ture on protoconch and first 0.25 teleoconch whorl. Sub- 
sequent whorls with median and peripheral bands of opaque 
white that are regularly interrupted by V-shaped, spirally 
dislocated axial bands of yellowish brown, axial bands 
extending as irregular zigzags across base. Columella 
opaque white. 

Protoconch 320 um wide, sculptured with few fine, crisp 
spiral threads. 

Teleoconch of 4.25 convex whorls, periphery suban- 
gulate, base gently rounded. First 1.75 whorls with 4 fine, 
crisp spiral threads on abapical half, abapical spiral bor- 
dering suture and persisting throughout, others progres- 
sively weakening and vanishing, the last vanishing at end 
of 2nd whorl. Three fine spiral threads on outside of col- 
umella. Columella thick, vertical. Aperture subcircular. 
Outer lip thin, inner lip thick, parietal glaze thin. Collabral 
growth lines prosocline on spire, sigmoidal on base. 

Animal unknown. 


Type data: Holotype MNZ M.247716 (3.35 x 2.75 mm, 
4.25 teleoconch whorls) and juvenile paratype MNZ: BS 
884 (0.630), 32°32.6'S, 167°29.2'E, summit of Wanganella 
Bank, Norfolk Ridge, dead, 133 m, r.v. Tangaroa. 


Distribution: Wanganella Bank, southern Norfolk Ridge, 
133 m (dead). 


B. A. Marshall, 1993 


Page 197 


Explanation of Figures 51 to 56 


Figures 51-54. Kaiparathina daedala Marshall, sp. nov., holotype radula. Figure 51. Entire width. Figures 52-54. 


Details of central and lateral teeth. 


Figures 55, 56. Kaiparathina coriolis Marshall, sp. nov., holotype jaw, ventral (interior) surface, anterior edge at 
top. Figure 55. Jaw width 1.60 mm. Figure 56. Detail of jaw elements of anterior edge. Scale Figures 51, 52, 53, 


56 = 100 um, Figure 54 = 25 um. 


Remarks: Kaiparathina fasciata differs from the holotype 
of K. navakaensis by being much thinner-shelled, by having 
a more excert protoconch and slightly, but distinctly, more 
strongly convex whorls, and by color pattern. It differs 
from K. boucheti by having a substantially smaller pro- 
toconch (width 320 wm instead of 400-420 um), by being 
more weakly and sparsely sculptured, and by having a 


color pattern on the teleoconch. It differs from K. prae- 
cellens by being thinner-shelled, more narrowly conical, 
and smaller in size relative to the number of whorls. Kai- 
parathina fasciata is substantially smaller than K. coriolis, 
which also differs in details of sculpture, color and color 
pattern. 


Etymology: Banded (Latin). 


Page 198 


Kaiparathina daedala Marshall, sp. nov. 
(Figures 30, 32, 33, 35, 36, 38, 40, 41, 51-54) 


Description: Shell up to 4.65 mm high, usually higher 
than broad, spire 0.9-1.2x as high as aperture, anom- 
phalous, of moderate thickness, glossy, nacreous within. 
Protoconch tip purplish brown. Teleoconch color variable. 
Holotype: first 2 whorls translucent white, subsequent 
spire whorls and base pinkish buff with narrow supra- 
and subsutural bands; suprasutural band (on peripheral 
keel) of reddish brown spots, subsutural band white; scat- 
tered reddish brown spots on base. Paratype with supra- 
median and suprasutural (on peripheral keel) rows of 
pinkish gray spots, ground color predominantly white over 
adapical half of whorl and pale pinkish gray below and 
on base, the latter mottled in paler and darker shades. 
Inner lip white, rim darkly pigmented. 

Protoconch 370 um wide, sculptured with 3 fine, crisp 
spiral threads, otherwise smooth. 

Teleoconch of up to 4.7 convex whorls; periphery be- 
coming rounded on last adult whorl, broadly angulate 
before; base weakly convex. First 2 spire whorls sculptured 
with 4 rounded spiral threads that may multiply by in- 
tercalation to number 6, adapical margins sharply defined; 
abapical spiral becoming strongest, persisting as peripheral 
keel, adapical margin exposed on spire; other spirals weak- 
ening late on 2nd whorl and vanishing early on 3rd whorl, 
spiral bordering peripheral spiral sometimes (paratype) 
persisting throughout. Subsequent whorls smooth apart 
from obscure spiral lines, and collabral growth lines; in 
paratype, however, 13 similar, rounded spiral threads re- 
solve on last half of last adult whorl. Base with 14-16 
rounded spiral threads, most of those on outer third re- 
solving on last half of last adult whorl. Collabral growth 
lines shallowly sigmoidal on spire, more deeply sigmoidal 
on base. Aperture subquadrate; outer lip thin at rim, thick- 
er and simple within; inner lip thick, parietal glaze very 
thin. 

Animal (reconstituted): operculum and jaws similar to 
those of Kazparathina boucheti and K. coriolis. 

Radula (Figures 51-54). Central tooth similar to that 
in Kaiparathina coriolis, lateral (5 pairs) and marginal 
teeth similar to those in K. vaubani. 


Type data: Holotype MNHN (4.65 x 3.80 mm, 4.70 
teleoconch whorls), Marion-Dufresne cruise 32 sta. CP57, 
21°05'S, 55°11’E, off Réunion, alive, 210-227 m. Paratype 
MNHN (4.05 x 3.80 mm, 4.30 teleoconch whorls), Mar- 
ion-Dufresne cruise 32 sta. DC 128, 20°51'S, 55°36’E, off 
Réunion, dead, 280-340 m. 


Distribution: Off Reunion, 210-340 m, living at 210- 
227 m. 


Remarks: Kaiparathina daedala is distinctive in having 
numerous spiral threads on the base. The terminal cusp 
of the central tooth is small as in K. coriolis instead of 
stilletto-like as in K. boucheti and K. vaubani. 


The Veliger, Vol. 36, No. 2 


ACKNOWLEDGMENTS 


For the loan of material I am grateful to P. Bouchet (Mu- 
seum National d’Histoire Naturelle, Paris), F. Collier 
(National Museum of Natural History, Washington, D.C.), 
J. A. Grant-Mackie (Auckland University), D. G. Herbert 
(Natal Museum, Pietermaritzburg), and P. A. Maxwell 
(Waimate, New Zealand). I thank B. Burt and W. St. 
George (Institute of Geological and Nuclear Sciences, 
Lower Hutt) and R. Thompson (Victoria University, Wel- 
lington) for access to scanning electron microscopes, and 
L. Quirk (Victoria University) for critical point drying. 
Thanks also to J. Lord for photography and L. Williams 
for manuscript processing. For constructive comments on 
the manuscript I am grateful to my colleagues D. G. Her- 
bert, J. H. McLean (Los Angeles County Museum of 
Natural History), and A. Waren (Natural History Mu- 
seum, Stockholm), and an anonymous reviewer. 


LITERATURE CITED 


Beu, A. G. 1973. Descriptions of new species and notes on 
taxonomy of New Zealand Mollusca, No. 2. Journal of the 
Royal Society of New Zealand 3:307-332. 

Beu, A. G. & P. A. MAXWELL. 1990. Cenozoic Mollusca of 
New Zealand. New Zealand Geological Survey Paleonto- 
logical Bulletin 58:1-518. 

DESHAYES, G. P. 1863. Conchyliologie de I’lle de la Reunion 
(Bourbon). Appendix E. Jn: L. Maillard, Notes sur L’lle de 
la Reunion, pp. 1-144. Dentu: Paris. 

FLEMING, C. A. 1966. Marwick’s illustrations of New Zealand 
shells, with a checklist of New Zealand Cenozoic Mollusca. 
New Zealand Department of Scientific and Industrial Re- 
search Bulletin 173:1-456. 

Hain, S. 1990. The benthic seashells (Gastropoda and Bivalvia) 
of the Weddell Sea, Antarctica. Reports on Polar Research 
70:1-180. 

HICKMAN, C. S. & J. H. McLean. 1990. Systematic revision 
and suprageneric classification of trochacean gastropods. 
Natural History Museum of Los Angeles, Science Series 35. 
169 pp. 

Jones, B. G. 1970. Paleoentology and paleoecology of Pakau- 
rangi Point, Kaipara, New Zealand. Transactions of the 
Royal Society of New Zealand. Earth Sciences 7(9):137- 
176. 

Lapp, H. S. 1982. Cenozoic fossil molluscs from western Pa- 
cific Islands: gastropods (Eulimidae and Volutidae through 
Terebridae). United States Geological Survey Professional 
Paper 1171:1-100. 

Laws, C.R. 1941. The molluscan faunule at Pakaurangi Point, 
Kaipara. No. 2. Transactions of the Royal Society of New 
Zealand 71:134-151. 

McLEaNn, J.H. 1982. Importance of gill structure in trochacean 
classification. Western Society of Malacologists, Annual Re- 
port 14:11 (abstract). 

MARSHALL, B. A. 1988. Thysanodontinae: a new subfamily of 
the Trochidae (Gastropoda). Journal of Molluscan Studies 
54:215-229. 

WarEN, A. 1990. Ontogenetic changes in the trochoidean (Ar- 
chaeogastropoda) radula, with some phylogenetic interpre- 
tations. Zoologica Scripta 19(2):179-187. 

WENZ, W. 1938-1944. Gastropoda. Teil 1: Allgemeiner Teil 
und Prosobranchia. Jn: O. H. Schindewolf (ed.), Handbuch 
der Paldozoologie 6(1):1-1639. Borntraeger: Berlin. 


The Veliger 36(2):199-202 (April 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


NOTES, INFORMATION & NEWS 


Prey Attack by the Patagonian Octopus 
Octopus tehuelchus d’Orbigny: an Odd Pattern 
by 
Oscar Iribarne, Miriam Fernandez 
School of Fisheries, 

WH-10, University of Washington, 
Seattle, Washington 98195, USA 
Marina Diaz 
Universidad Nacional del Sur, 
Bahia Blanca, Argentina 
and 
Marina Clemente 
Universidad Nacional de Buenos Aires, 
Buenos Aires, Argentina 


Introduction 


Most octopus species are opportunistic (MANGOLD, 1983; 
AMBROSE, 1984) and versatile predators that use different 
techniques to overcome their prey: (1) some crab prey are 
killed with a toxin (NIXON & BOYLE, 1982); (2) hermit 
crabs can be either pulled from their shells (FAWCET, 1984; 
Brooks & MaArISCAL, 1985) or their shells can be drilled 
(WoDINSKY, 1969); and (3) shelled mollusks are usually 
drilled, although some are killed by pulling apart their 
valves (FUJITA, 1916; PILSON & TaAyLor, 1961; ARNOLD 
& ARNOLD, 1969; HARTWICK et al., 1978). 

Octopus tehuelchus d’Orbigny, a small-sized species dis- 
tributed along the southwestern Atlantic (CARCELLES, 1940; 
CASTELLANOS & MENNI, 1969), reaches high densities in 
the intertidal and shallow subtidal zones (up to 15 m depth) 
of the San Matias Gulf, Argentina (41°S; IRIBARNE, 1990). 
In contrast with other octopus species, it is not a generalist 
predator (IRIBARNE ef al., 1991). Either the hard shells or 
chemical defenses of prey appear to be the main octopus 
deterrents (IRIBARNE et al., 1991). 

In this note we report that the Patagonian octopus over- 
comes hermit crabs (Pagurus sp.) by drilling the gastropod 
(Tegula patagonica d’Orbigny) valves used as shelter but 
never drills the shell when attacking the living gastropod 
(T. patagonica) itself. Implications of this pattern of attack 
are discussed. 


Materials and Methods 


This study was conducted under laboratory conditions with 
octopuses and prey species collected in the San Antonio 
Bay, northern Patagonia, Argentina (41°S, 63°30’W). Oc- 
topus tehuelchus, the gastropod Tegula patagonica, and the 
hermit crab Pagurus sp. are commonly found in the study 
area. Shells of 7. patagonica are the most common shelter 
used by hermit crabs Pagurus sp. in this area (personal 


observations, Iribarne and Fernandez) and both are prey 
of the Patagonian octopus (personal observations, Iribarne 
and Fernandez). Octopus and potential prey species were 
collected by diving, taken to the laboratory, and held in 
60-L seawater tanks with temperature and salinity close 
to field conditions. The water was exchanged every other 
day to eliminate nitrogenous wastes. Brooding females were 
discarded due to low feeding activity (POLLERO & IrRI- 
BARNE, 1988). Before each trial octopuses were starved for 
24 hr and weighed. Shells of living gastropods were mea- 
sured (total height) and hermit crab shelters were mea- 
sured (total height) and scrutinized for evidence of octopus 
drilling to avoid using already drilled hermit crab shelters. 
Independent experiments were conducted with each prey 
species. Octopuses (17 to 56 g) were offered two individuals 
of T. patagonica, equally distributed between two size class- 
es (<10 mm and >10 mm height; replicated 10 times) or 
with two individuals of hermit crabs Pagurus sp. living in 
T. patagonica shell, one of each size class (<10 mm and 
>10 mm height; replicated 12 times). After 24 hr prey 
remains were carefully scrutinized with a binocular mi- 
croscope for evidence of drilling. When holes were present 
the major axis (diameter) of the external border of the 
bored hole was measured to 0.01 mm. 


Results and Discussion 


Twenty percent of the Tegula patagonica offered were con- 
sumed but none of them drilled. Fifty-five percent of the 
hermit crabs sheltering in the 7. patagonica were consumed 
and all the gastropod shells were drilled. Most holes were 
found in the second whorl of the shell, but some were 
located in the spire closer to the last whorl or in the last 
whorl. In 20% of the cases octopuses made two holes in 
different whorls, both perforating the shell. It is unknown 
which hole was bored first. The outer diameter of the holes 
ranged from 0.35 to 0.59 mm (x = 0.46, SD = 0.087, n 
= 13) and was not correlated with octopus weight (7 = 
0.55, df = 11) or shelter size (r = 0.2, df = 11). The 
diameter of the hole decreased from the external border 
towards the internal cavity as occurs with O. vulgaris Cu- 
vier drilling Mytilus edulis Linnaeus (NIXON, 1979), Pitaria 
chione Linnaeus, and Venus verrucosa Linnaeus (AMBROSE 
& NELSON, 1983). Drilling on hermit crabs has been pre- 
viously reported by WODINSkKY (1969). Hermit crabs re- 
duce predation by a variety of behavioral means, the sim- 
plest one being retraction into the shell (KOBAYASHI, 1986). 
The relatively high number of double complete holes may 
indicate a high rate of failure in the attacks. 

Octopus predation on mollusks has been inferred from 
prey remains based on the presence of bore holes (ROBBA 
& OSTINELLI, 1975; STANTON & NELSON, 1980; FAWCET, 


Page 200 


1984; Evans, 1980-1981; VERMEIJ, 1987). Our results 
show that hermit crabs are preyed upon by drilling shells 
of Tegula patagonica, which interestingly were never drilled 
when the gastropod was the prey. This result contrasts 
with those found for Octopus sp. and Tegula funebralis 
Adams along the northeastern Pacific coast, where the 
gastropod is always drilled, but drilling is unlikely when 
T. funebralis shells are inhabited by hermit crabs (FAWCET, 
1979). These different outcomes suggest that caution should 
be exercised when octopus predation on gastropods is in- 
ferred from prey remains. 


Acknowledgments 


We thank N. Dieu, S. Acosta, A. de Cacho, T. Cacho, 
and E. Zampatti for technical assistance. Dr. B. Marcy, 
Dr. G. Vermeij, and P. Wardrup made valuable comments 
on the manuscript. The work was supported by the Rio 
Negro Province and the Universidad Nacional del Coma- 
hue, Argentina. 


Literature Cited 


AMBROSE, R. 1984. Food preferences, prey availability, and 
the diet of Octopus bimaculatus Verrill. Journal of Experi- 
mental Marine Biology and Ecology 77:29-44. 

AMBROSE, R. F. & B. V. NELSON. 1983. Predation by Octopus 
vulgaris in the Mediterranean. Marine Ecology 4:251-261. 

ARNOLD, J. M. & K.O. ARNOLD. 1969. Some aspects of hole- 
boring predation by Octopus vulgaris. American Zoologist 
9:991-996. 

Brooks, W. R. & R. M. MariscaL. 1985. Protection of the 
hermit crab Pagurus pollicaris Say from predators by hydroid- 
colonized shells. Journal of Experimental Marine Biology 
and Ecology 87:111-118. 

CARCELLES, A. 1940. Catalogo de los moluscos marinos de 
Puerto Quequen (Rep. Argentina). Revista del Museo de 
La Plata Seccion Zoologia, pp. 2-227. 

CaSTELLANOS, Z. A. DE & R.C. MENNI. 1969. Sobre dos pulpos 
costeros de la Argentina. Neotropica 15:89-94. 

Evans, R. A. 1980-1981. Octopus predation on Cypraea spadi- 
cea. Of Sea and Shore 11:225-226. 

FawceT, M. H. 1979. The consequences of latitudinal vari- 
ation in predation for some marine intertidal herbivores. 
Ph.D. Dissertation, University of California, Santa Barbara, 
California, USA. 

FawceT, M. H. 1984. Local and latitudinal variation in pre- 
dation on an herbivorous marine snail. Ecology 65:1214- 
1230. 

Fujita, S. 1916. On the boring of the pearl oyster by Octopus 
(Polypus) vulgaris Lamarck. Dobutsugaku Zasshi 28:250- 
25 ile 

Hartwick, E. B., G. THORARINSSON & L. TULLOCH. 1978. 
Methods of attack by Octopus dofleini (Wulker) on captured 
bivalve and gastropod prey. Marine Behavior and Physiology 
5:193-200. 

IRIBARNE, O. 1990. Life history and distribution of the small 
south western Atlantic octopus, Octopus tehuelchus. Journal 
of Zoology, London 223:549-568. 

IRIBARNE, O., M. FERNANDEZ & H. ZuccHINI. 1991. Prey 
selection by the small Patagonian octopus, Octopus tehuelchus 
dOrbigny. Journal of Experimental Marine Biology and 
Ecology 148:271-281. 


The Veliger, Vol. 36, No. 2 


KopayasHI, D. R. 1986. Octopus predation on hermit crabs: 
a test of selectivity. Marine Behavior and Physiology 12: 
125-131. 

MANGOLD, K. 1983. Octopus vulgaris. Pp. 157-200. In: P. R. 
Boyle (ed.), Cephalopod Life Cycles. 2. Comparative Stud- 
ies. Academic Press: London. 

Nixon, M. 1979. Hole-boring in shells by Octopus vulgaris 
Cuvier in the Mediterranean. Malacologia 18:431-443. 
NIxon, M. & P. BoyLe. 1982. Hole-drilling in crustaceans by 
Eledone cirrhosa (Mollusca: Cephalopoda). Journal of Zo- 

ology, London 196:439-444. 

Pitson, M. E. Q. & P. B. TayLor. 1961. Hole drilling by 
Octopus. Science 134:1366-1368. 

POLLERO, R. & O. IRIBARNE. 1988. Biochemical changes during 
the reproductive cycle of the the small Patagonian octopus, 
Octopus tehuelchus, d’Orb. Comparative Biochemistry and 
Physiology B 90:317-320. 

Rossa, E. & F. OSTINELLI. 1975. Studi paloecologici sul plio- 
cene Ligure: I. Testiomonianze di predazione sui molluschi 
Phiocenici di Albenga. Rivista Italiana di Paleontologia 81: 
309-373. 

STANTON, R. J. & J. R. NELSON. 1980. Reconstruction of the 
trophic web in paleontology: community structure in the 
Stone City Formation (Middle Eocene, Texas). Journal of 
Paleontology 54:118-135. 

VERMEIJ, G. J. 1987. Evolution and Escalation: An Ecological 
History of Life. Princeton University Press: Princeton, New 


Jersey. 
WoopInsky, J. 1969. Penetration of the shell and feeding of 
gastropods by Octopus. American Zoologist 9:997-1010. 


Examples of Damage Repair in the Shell of the 
Cephalopod Genus Argonauta 
by 
Kent D. Trego 
3895 LaSelva Dr., 
Palo Alto, California 94306 


ARNOLD (1985) reported on damage and subsequent repair 
in the shell of the cephalopod Nautilus pompilius Linnaeus, 
1758. This study was important in understanding the life 
history of Nautilus, specifically, predation on it. The ceph- 
alopod genus Argonauta comprises a group of octopods that 
utilize a thin unichambered exoshell, which functions as 
an egg case and is carried for only a short duration com- 
pared to the lifetime shell of Nautilus. While not having 
the significance of the phenomenon in the Nautilus shell, 
breakage and repair do occur in the Argonauta shell. Ex- 
amples of damage and repair in the Argonauta shell are 
briefly discussed here. 

There are two types of abnormal growth in Argonauta 
shells. One of these abnormalities is nonsymmetrical growth 
of the shell. The shell is created by secretions from two 
lobes on the number one arm pair of the female animal. 
Irregular secretion rates of the lobes result in nonsym- 
metrical shells (Figure 1A). The common results of non- 
symmetrical growth in Argonauta shells are uneven tu- 
bercle lengths of the two keels on the back of the shell and 
different structures of the two tips of the aperture (Figure 


Notes, Information & News 


Page 201 


Figure 1 


A. Examples of nonsymmetrical Argonauta shells showing different structures of the tips of the aperture at the 
umbilical region of the shell. At left is a side view of a specimen of A. argo (225 mm) and at right is an apertural 
view of a specimen of A. nodosa (210 mm). The tips of the aperture at the umbilical region of the shells are indicated 
by arrows. B. A specimen of A. argo (115 mm) with shell repair at the early whorl of the shell, resulting in an 
abnormal flattening of the early whorl structure. The repaired area of the shell is indicated by the arrow. C. A 
specimen of A. argo (145 mm) with shell repair on the keel region of the shell, resulting in a depression on the 
backside of the shell. The depression area of the shell is indicated by the arrow. D. A specimen of A. nodosa (216 
mm) with damage and continual shell secretion at the aperture area of the shell. The growth scar is indicated by 


arrows. 


1A) where the aperture meets the umbilical region of the 
shell. 

The second type of abnormal growth on Argonauta shells 
results from shell damage and repair by the female. Severe 
shell damage can result in patching of the shell, which 
does not include resumption of the shell pattern. The 
patching may result in the reattachment of broken shell 
fragments. An example of such shell damage is shown in 
Figure 1B, where a shell of the species Argonauta argo 


Linnaeus, 1758, has been repaired in the early whorl of 
the shell. The shell patch is flat and the normal curving 
structure of the early whorl is not recreated. Less traumatic 
shell breakage and repair will result in the resecretion of 
the shell’s normal pattern. Examples of this less traumatic 
shell damage and repair are shown in Figure 1C, D. In 
Figure 1C, damage to the keel area of a specimen of A. 
argo has resulted in a depression in the backside of the 
shell. A specimen of Argonauta nodosa Lightfoot, 1786, is 


Page 202 


The Veliger, Vol. 36, No. 2 


shown in Figure 1D. This shell has experienced damage 
and continual secretion of the shell at the aperture area of 
the shell. 

ARNOLD (1985) concluded that massive mechanical shell 
damage to the shell of Nautilus pompzlius could be rectified 
by the animal. It appears that similar damage to the shell 
of the female Argonauta can also be successfully corrected 
by the animal. The cause of shell damage in Nautilus is 


largely predation (ARNOLD, 1985) and I assume that pre- 
dation is also largely responsible for the shell damage in 
Argonauta. 


Literature Cited 


ARNOLD, J. M. 1985. Shell growth, trauma, and repair as an 
indicator of life history of Nautilus. The Veliger 27:386-396. 


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CONTENTS — Continued 


Formation of organic sheets in the inner shell layer of Geloina (Bivalvia: Cor- 
biculidae): an adaptive response to shell dissolution 
SHIN JT DSA JW 5.0 shige act Pes ig SON eae) ge ep euch eo hea Gf eee sa 


A new species of Cypraea from Samoa in the C. cribraria complex 
CG. M."BURGESS 45; ie Seis Wie oe ea eee ooo Ls ee 


How does Strombina reproduce? Evidence from two Venezuelan species (Proso- 
branchia: Columbellidae) 
ROBERTO CIPRIANI AND PABLO E. PENCHASZADEH ...................- 


A review of the genus Kaiparathina Laws, 1941 (Mollusca: Gastropoda: Tro- 
choidea) 
BRUCE: A: MIARSHATT 9 oclso 00 Vy 2k Ses Br ite eee er 


NOTES, INFORMATION & NEWS 


Prey attack by the Patagonian octopus Octopus tehuelchus d’Orbigny: an odd 
pattern 

OSCAR IRIBARNE, MIRIAM FERNANDEZ, MARINA DIAZ, AND MARINA CLE- 

MMEINGIEES 5c 80. ait aap So actge devs ipa ec yan Ohad pee aC Sate A Si ge 


Examples of damage repair in the shell of the cephalopod genus Argonauta 
KENTHD iy PREGGO G Gia 5 cade gr i aia) ek Rane eon a a rr 


ave 


VELIGER 


A Quarterly published by 

CALIFORNIA MALACOZOOLOGICAL SOCIETY, INC. 
Berkeley, California 

R. Stohler, Founding Editor 


Volume 36 auilyaleed 993 


CONTENTS 


Energetic implications of variation in pedal mucus production by Patella vulgata 
Linnaeus, 1758 


IMIAIRES Sia LDUAWAIIS ore oat tale at, ello ecg teh nn RP ene 203 
Application of a two-dimensional electrophoresis method to the systematic study 
of Notaspidea (Mollusca: Opisthobranchia) 
RVOKOMISUBOKAWAAND: JiUN-TCHT MIVAZAKE §. 2 54s. eee ee 209 
Karyotype and nucleolus organizer regions in Ostrea puelchana (Bivalvia: Os- 
treidae) 
ANA INSUA AND CATHERINE THIRIOT-QUIEVREUX ..................... 215 
Variability in growth and age structure among populations of ribbed mussels, 
Geukensia demissa (Dillwyn) (Bivalvia: Mytilidae), in Jamaica Bay, New 
York (Gateway NRA) 
DAVID EK RANZ VANDI | OHN@ I (LANACREDE 352.050 2 eee es ee ee 220 
Maturation processes in female Loligo bleekeri Keferstein (Mollusca: Cephalo- 
poda) 
GYEONG HUN BAEG, YASUNORI SAKURAI, AND KENJI SHIMAZAKI ........ 228 
A comparison of larval development, growth, and shell morphology in three 
Caribbean Strombus species 
MEGAN Davis, CYNTHIA A. BOLTON, AND ALLAN W. STONER .......... 236 


CONTENTS — Continued 


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The Veliger 36(3):203-208 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Energetic Implications of Variation in Pedal Mucus 


Production by Patella vulgata Linnaeus, 1758 
by 


MARK S. DAVIES! 


Department of Environmental Biology, University of Manchester, Manchester, M13 9PL, UK 


Abstract. The important role played by pedal mucus production in the flow of energy within intertidal 
mollusks has been recognized. However, thus far, intraspecific variation in mucus production has not 
been considered. This study demonstrates that mucus production varies both spatially and temporally. 
Mucus production rates by immersed limpets, Patella vulgata Linnaeus, 1758, from one population 
showed temporal variation of up to about five-fold. A population of high-shore limpets produced mucus 
at about twice the rate of mid- and low-shore populations. Limpets on a semi-exposed shore produced 
mucus at about 1.5 times the rate of those on a moderately sheltered shore. These differences may be 
due to spatial differences in activity. When stationary, limpets secrete adhesive mucus only within the 
first 10 min of attachment and mucus production is proportional, as expected, to animal weight”. Spatial 
and temporal differences between conspecific populations in terms of an energetically important process 
(mucus production) will produce differences in energy balance. The results are discussed in terms of 
the important consequences of variation in physiological processes to the description of energy flow and 


the concept of the “energy budget.” 


INTRODUCTION 


Carefully compiled descriptions of energy flow or “energy 
budgets” can help to produce an understanding of energy 
transfer through ecosystems. Such studies focused on in- 
tertidal grazers (see HAWKINS & HARTNOLL, 1983, for 
review) can show the importance of these species in terms 
of energy flow within the littoral community. Recently, 
however, it has been realized that many such studies in- 
volving marine mollusks, particularly gastropods, are in- 
complete. Numerous works (EDWARDS & WELSH, 1982; 
Horn, 1986; PECK et al., 1987; DAVIEs et al., 1990a) have 
discovered that mucus, which was hitherto ignored, can 
play an important role in the energetics of these species, 
comprising up to 70% of consumed energy (HorRN, 1986). 
However, in each case mucus was measured under one set 
of conditions only and no attempt was made to discover 
any variation in its production or the factors which may 
be responsible for this. 

In gastropods most mucus is produced for use in loco- 
motion where, in Littorina littorea, DAVIES et al. (1992a) 
showed its cost in energy terms to be over 35 times that 


' Present address: The Marine Biological Association of the 
UK, Citadel Hiil, Plymouth, PL1 2PB, UK. 


of the metabolic cost of locomotion. Although mollusks 
might be expected to produce mucus at a functionally 
minimal level, it must be recognized that mucus may have 
functions other than locomotion (e.g., as a protective bar- 
rier, or in trail following, see DENNY, 1989). Because the 
roles these functions play in molluscan biology are likely 
to vary with environmental factors (including pollution, 
DavIEs, 1992), the same rates of mucus production might 
not be expected to be shown by different populations. This 
is particularly likely when locomotory activity differs be- 
tween populations (see LITTLE, 1989). 

This paper aims to demonstrate that caution should be 
exercised in interpreting the results from ecophysiological 
studies, such as those on mucus production, owing to the 
labile nature of physiological processes themselves. Despite 
its historical omission from energy budgets, the simple 
insertion of a “mucus” term into a budget could be erro- 
neous unless the variability of mucus production with en- 
vironmental factors has been assessed. Using the limpet 
Patella vulgata Linnaeus, 1758, as an example organism, 
I aimed to investigate how the production of an energet- 
ically expensive product, mucus, can vary intraspecifically 
both spatially and temporally, and what might cause that 
variation. Results are reported of experiments assessing 
variation in immersed mucus production from one popu- 


Page 204 


The Veliger, Vol. 36, No. 3 


-2.5 
2 
wo 
= eV) January 1990 
2 
Cee June 1988 
rome 
ek -35 
ayes February 1989 
3D 
E > 4.0 April 1990 
8 ne) 
o 2 
Q 
7 AG 
io August 1989 


-5.0 
-1.0 -0.5 0.0 0.5 1.0 1.5 


Log,, whole animal dry weight (g) 
Figure 1 


Temporal variation in pedal mucus production rates by Patella 
vulgata immersed in seawater. Regression data given in Table 1. 


lation over time and variation between populations whose 
habitats differ in shore height and wave exposure. In ad- 
dition, since many populations of P. vulgata spend a large 
proportion of their time inactive (see HARTNOLL & 
WRIGHT, 1977; LITTLE, 1989), the timing of mucus pro- 
duction during this stationary phase was investigated by 
recording pedal mucus secretion after increasing periods 
of attachment. When limpets are stationary, the amount 
of mucus they produce may be a function of pedal area, 
since the pedal sole is the site of secretion of the adhesive 
mucus (GRENON & WALKER, 1978). Thus stationary mu- 
cus production should be a function of animal weight” 
since foot area grows in isometric proportion to weight 
(unpublished data). This can be tested using my experi- 
mental data. 


MATERIALS anp METHODS 


When collecting Patella vulgata, both the animal and the 
rock on which it was situated were removed and taken to 
the laboratory. Limpets were then easily lifted from the 
rock after they had moved away from their home scars. 
Experiments on limpets from the Isle of Man were per- 
formed at Port Erin, Isle of Man within 12 hr of collection. 


The experimental apparatus consisted of a large glass plate 
in a shallow tank into which fresh seawater flowed con- 
tinually. The temperature of the water was maintained at 
10°C. To assess pedal mucus production by immersed lim- 
pets, the foot of each animal was gently scraped free of 
feces, mucus, and other debris, and the animal placed in 
the center of the plate. After 6 hr (the mean time of im- 
mersion or emersion by the tide at MTL) each was re- 
moved from the plate, its foot scraped clean of mucus with 
a single sweep of the rounded end of a pair of forceps 
(DAVIES et al., 1990a), and the mucus added to that ad- 
hering to the plate. A razor blade was used to scrape the 
plate free of mucus and the mucus was dried at 70°C and 
weighed to 0.1 mg. The dry weights of limpet shell and 
flesh were separately determined and summed to give whole 
animal dry weight. 

To study the temporal range of mucus production rates 
exhibited by one population, pedal mucus production rates 
of immersed limpets were determined as above for limpets 
collected from MTL at Derbyhaven, Isle of Man (Grid 
Reference SC 294 685) in June 1988, February 1989, 
August 1989, January 1990, and April 1990. The shore 
is moderately sheltered and rates about five on BAL- 
LANTINE’s (1961) scale of exposure. This scale grades shores 
from ‘“‘one” (extremely exposed) to “eight” (extremely 
sheltered) depending on the biota present. Sample sizes 
ranged from 10 to 50 animals. 

The effect of shore height was examined by determining 
pedal mucus production rates for 20 animals collected each 
from horizontal surfaces at high-shore, MTL, and low- 
shore at Derbyhaven in February 1989. The effect of wave 
exposure on mucus production was assessed using samples 
of 20 Patella vulgata collected in February 1989 from hor- 
izontal surfaces at mid-shore at both Port St. Mary, Isle 
of Man (Grid Reference SC 208 669), a semi-exposed 
shore which rates about four on BALLANTINE’s (1961) 
scale, and St. Michael’s Island, Isle of Man (Grid Ref- 
erence SC 294 674), a very sheltered shore which rates 
about seven. 

Limpets used to determine when during the 6-hr (at 
MTL) stationary period the adhesive pedal mucus is se- 
creted were collected from MTL at Rhosneigr, Angle- 
sey, Wales (Grid Reference SH 314 729) in November 
1989. They were transported to the laboratory at Man- 


Table 1 


Calculated relationships between pedal mucus production rate (y, g dry weight hr~') and whole animal dry weight 
(x, g) for Patella vulgata immersed in seawater. Temporal variation. Ranges given are SE. 


Equation n ie P 
June 1988 V2 DAT X TN Oe 22S OFXt MO meine o eee ool 50 0.569 <0.001 
February 1989 y= EOT25X) 1Ome eo ell xl Om Seine 378- 0.03 20 0.503 <0.001 
August 1989 y= SONG WOR Ey 2 Om a O misoca ail OC2k 20 0.767 <0.001 


January 1990 O50" x On: 


lI 


st A/a eal Oimmicuc eet 0058 10 0.448 <0.05 
April 1990 y=" 1-202) X10 N66 xl Ono 20-924= 0-028 30 0.349 


M. S. Davies, 1993 


chester, maintained in an artificial tidal system (on a 6-hr 
immersion, 6-hr emersion cycle) and used within four days. 
Limpets were placed singly on small glass plates for periods 
of 1, 2, 3, 5, 10, 20, and 30 min and 1, 2, 4, and 6 hr in 
an environment of 10°C and 70% relative humidity. After 
the allotted time the limpets were removed and the pedal 
mucus produced was collected and measured as before. 
Sample sizes in each time period were nine or ten limpets. 


RESULTS 


There is wide variation (up to above five-fold) in pedal 
mucus production rate by immersed Patella vulgata from 
Derbyhaven depending on the date of measurement (Fig- 
ure 1). The regression lines constructed for data collected 
in February 1989, January 1990, and April 1990 have 
the same elevation (intercept) (ANCOVA, F,,, = 0.9, P 
> 0.5), but the June 1988 line shows a significantly higher 
elevation (Fo, = 14.9, P < 0.001) and the August 1989 
line a significantly lower elevation (F;;, = 4.2, P < 0.02). 
Thus mucus production rate was greatest when assessed 
in June 1988 and least in August 1989, with those as- 
sessments in February 1989, January 1990, and April 
1990 of intermediate value. The slopes of each regression 
line (Table 1) are, however, not significantly different 
(Fy, = 0.7, P > 0.1)—ze., the way in which mucus 
production scales with whole animal dry weight did not 
vary between sampling dates. 

Immersed pedal mucus production rate varies with both 
wave exposure and shore height (Figure 2, Table 2). Lim- 
pets at mid-shore at Port St. Mary (semi-exposed shore) 
secreted mucus at about 1.5 times the rate (Ff, ,, = 4.8, P 
< 0.05) of those on the more sheltered shore at MTL at 
Derbyhaven (moderately sheltered). No significant cor- 
relation was found between mucus production rate and 
whole animal dry weight for the limpets from mid-shore 
at St. Michael’s Island (very sheltered shore). At Derby- 
haven, limpets high on the shore produced mucus at about 
twice the rate of those at MTL or those low on the shore 
(F,5, = 8.1, P < 0.002). These latter groups of animals 
secreted mucus at rates which are not significantly different 


Page 205 


-2.5 


-3.0 


high 


-3.5 


semi-exposed 


(g dry weight h-" ) 


-4.0 


Log,, pedal mucus production rate 


-0.5 0.0 0.5 1.0 1.5 2.0 


Log,. whole animal dry weight (g) 
Figure 2 


Pedal mucus production rates by immersed Patella vulgata col- 
lected from four shore positions: high-, mid-, and low-shore on 
moderately sheltered shore, mid-shore on semi-exposed shore. 
Regression data given in Table 2. 


from each other (F, 3, = 0.9, P > 0.1). The slopes of the 
regression lines in Figure 2 do not differ significantly (F;,, 
= 0.5, P > 0.1) (mean slope = 0.611) showing that the 
way in which mucus production scales with animal size 
did not vary between limpets from different areas of shore 
(except at St. Michael’s Island). 

Pedal mucus produced by emersed limpets (animals sta- 
tionary) is independent of time after the first 10 min of 
attachment (Figure 3, Table 3). Note that Figure 3 and 
Table 3 express mucus in terms of weight produced and 
not as a rate of production. This distinction is important 
in actuarial bioenergetics (see RUSSELL-HUNTER & 
BUCKLEY, 1983). The regression lines in Figure 3 differ 
neither in slope (5, = 0.2, P > 0.1) nor elevation (F660 
= 1.4, P > 0.1). The mean exponent from Table 3 is not 
significantly different from the theoretical exponent (0.667) 
showing that limpet mucus production scales as expected 


Table 2 


Calculated relationships between pedal mucus production rate (y, g dry weight hr~') and whole animal dry weight (x, 
g) for immersed Patella vulgata collected from different shore heights at Derbyhaven (moderately sheltered shore) and 
from mid-shore at Port St. Mary (semi-exposed shore). Ranges given are SE. 


Equation n ie P 
Derbyhaven 
high-shore 209 OR XO ime aE 2s Ome icc 4830.02 20 0.578 <0.001 
mid-shore 9 = NOVA NO" ae Boil os WO poorer sesuen 20 0.503 <0.001 
low-shore i) = GSil 3 IO as WD 2 I reogeteoey 19 0.365 <0.001 
Port St. Mary 
mid-shore y = 1.175 x 1074 + 6.4 X 107% %07386+0.028 20 0.664 <0.001 


Page 206 


-2.5 

Cc 

2 

S 

3 -3.0 

2 

as 

2% 

® 

E > , E e e 
-J. ee 

Se 

Q 

2 @ 

D 

° 

25 


“0.0 0.5 1.0 1.5 
Log,. whole animal dry weight (g) 
Figure 3 


Pedal mucus production by Patella vulgata as a function of whole 
animal dry weight for animals left to adhere to glass in air at 
70% relative humidity for time periods from 5 min to 6 hr. Data 
points are for 5 min of attachment. Regression lines are for other 
periods (A = 10 min, B = 20 min, C = 30 min, D = 1 hr, E = 
2 hr, F = 4 hr, G = 6 hr). Regression data given in Table 3. 


with animal weight. One, 2, and 3 min experimental pe- 
riods did not result in the production of any mucus and 
limpets did not attach. After 5 min mucus was secreted 
and although there is no significant correlation between 
mucus production and whole animal dry weight, all the 
datum points (Figure 3) are below the other regression 
lines. Thus less mucus was produced than after 10 or more 
min. Only two out of the 10 experimental animals were 
found to be attached after 5 min, while after 10 min and 
longer experimental periods all the animals were firmly 
attached. 


DISCUSSION 


The results of this study must be considered with due 
regard to placing limpets in an artificial environment. Di- 


The Veliger, Vol. 36, No. 3 


rect extrapolation of laboratory behavior to the field is 
difficult and this must be borne in mind when the results 
are considered. Movement in the laboratory (less than 
=0.2 m from the center of the plate) was less than in the 
field observations of HARTNOLL & WRIGHT (1977) con- 
ducted at Derbyhaven (mean foraging distance = 0.4 m); 
and the substratum in the field is probably considerably 
rougher than the experimental substratum. Pedal mucus 
production rate by Haliotis tuberculata has been shown to 
increase with the particle size (roughness) of the substra- 
tum (CULLEY & SHERMAN, 1985). Because there was little 
water movement in the experimental tanks, little mucus 
would have been lost into the water. DAVIEs et al. (1992b) 
have shown that mucus decay in seawater is primarily due 
to the mechanical action of the seawater. 

The reasons for temporal variation in mucus production 
are unclear but may reflect activity differences produced 
by varying environmental conditions. Limpets may have 
moved less on the experimental plates in August than in 
June and the winter months. Tentatively, this could be 
because during late summer the gonad competes for space 
within the animal with the visceral mass, making loco- 
motion difficult (ORTON et al., 1956). DAVIES et al. (1990b) 
reported seasonal variation in the composition of Patella 
vulgata pedal mucus which may be related to the breeding 
cycle. 

The increases in pedal mucus production rate up shore 
and with wave exposure may reflect differences in limpet 
activity or imply mucus is secreted onto the sole at different 
rates depending on shore position. Both high-shore and 
exposed-shore limpets may have their foraging periods 
restricted by limited immersion time (assuming limpets 
only forage when the tide is in, as is the case at Derbyhaven, 
HARTNOLL & WRIGHT, 1977, and personal observations). 
and violent wave action, respectively. Thus when immersed 
in experimental tanks, limpets from these environments 
may attempt to maximize their food intake and so are more 
active than limpets from lower down the shore or from 
less exposed shores. Adjacent populations of limpets have 
been shown to differ markedly in foraging behavior (LITTLE 
et al., 1991). 


Table 3 


Calculated relationships between weight of pedal mucus produced (y, g dry weight) and whole animal dry weight (x, g) 
for Patella vulgata left to adhere to glass for time periods from 10 min to 6 hr. Ranges given are SE. t-value describes the 
goodness of fit of the calculated exponent to the theoretical exponent (0.667). 


Equation 

10 min Mi chia es NO ee uot ee IO 

20 min y = 25194" X N0mt = 2295=x 10m>- 

30 min y= "32631 10m a3 '2 1) xo Ose 

1 hr y = 2.630 x 10-* + 4.50 x 10->- 

2 hr y= 2251 2X Omi 4 ole xe Ome: 

4 hr y= 2:692 XK N0ee 327 xMlOn>: 

6 hr y = 4.677 x 10-* + 6.16 x 10->- 
mean exponent = 0.696 + 0.027, ¢ = 1.062, 0.2 < P < 0.5 


n r? IP 
0-617 0.065 10 0.529 <0.01 
40-7104 0.065 9 0.656 <0.01 
4¢0-600+0.051 10 0.638 <0.01 
40.694 + 0.088 9 0.498 <0.05 
¢0:853£0.114 10 0.413 <0.05 
40.791 0.075 10 0.584 <0.02 
40-606 -+0.050 10 0.407 <0.05 


M. S. Davies, 1993 


Page 207 


The reasons for the lack of correlation between mucus 
production and animal size only on the very sheltered shore 
are unclear. However, conditions on this shore are different 
from those on the more exposed shores. The very sheltered 
shore is dominated by fucoid algae, with limpets occurring 
singly (rather than in clumps, as on the other shores) 
underneath the algal canopy. The individual limpet for- 
aging pattern on this shore could be dependent more on 
microhabitat than on any factor affecting the shore as a 
whole. 

The lack of secretion of pedal mucus after the first 10 
min of attachment is not surprising. Since limpets are 
stationary, only enough mucus to facilitate adhesion will 
be secreted. This implies that mucus maintains its func- 
tional capability (adhesive properties) over at least 6 hr 
and that there are long periods during which the pedal 
secretory apparatus is inactive. The secreted mucus will 
be important in defense against predators because of its 
role in adhesion (DENNY, 1980). The scaling of mucus 
production with animal weight” suggests that “stationary” 
mucus is secreted from all areas of the sole. This contrasts 
with locomotory secretions which are thought to originate 
from the anterior groove (GRENON & WALKER, 1978). The 
results suggest that when assessing mucus production from 
stationary limpets (as may be done to obtain estimates of 
the energetic cost of mucus production) measurements need 
be taken after 10 min of attachment only and not after 
however long the animals are emersed zm situ. When lim- 
pets stop moving zm situ they may not secrete extra mucus 
for adhesion but use the mucus already secreted onto the 
pedal sole which facilitated their last movement. Thus the 
value of mucus production in an energy budget may be 
artificially increased by measuring stationary production 
(see DAVIES et al., 1990a). However, CONNOR (1986) found 
trail and stationary mucus from acmaeid limpets to have 
different properties (perhaps related to function), so per- 
haps a fresh layer of mucus is secreted at the start of a 
stationary period. 

The differential rates of mucus production reported in 
this study have important implications for the assessment 
of that component of energy flow which is mucus. A single 
measurement cannot embody temporal variation (see DA- 
VIES et al., 1990a) nor be extrapolated to other populations 
or even other species (see CALOW, 1974). The energy drain 
as mucus will differ between limpets from different pop- 
ulations and since mucus plays a large role in the physi- 
ological energetics of limpets (DAVIES et al., 1990a), the 
energy balance of these different populations will vary 
considerably. Although allometric effects make direct com- 
parisons between populations difficult, as an example of 
this variation a limpet of whole dry weight 10 g can be 
used. Assuming the calorific value of mucus measured by 
Davies et al. (1990a) (8.984 kJ g~') is valid for all mucus 
samples (but see DAVIES et al., 1990b), then depending on 
shore position and collection date examined in this study 

’ the energetic cost of mucus production by a 10 g immersed 
limpet varies from 2.5 to 11.6 J hr~'. In more conventional 


energy budget units, this is 10.9 to 50.8 kJ year~', assum- 
ing the limpet spends half its time submerged (DAVIES et 
al., 1990a). These values represent considerable propor- 
tions of the limpet energy budget: up to 21% of consumed 
energy for a limpet of whole dry weight 10 g (using data 
from DAVIES et al., 1990a, and WRIGHT & HARTNOLL, 
1981). This phenomenon has also been demonstrated by 
Horn (1986) for the ormer Haliotis tuberculata. Thus as- 
sessments of energy flow should be regarded as “snapshots” 
whose comparative usefulness is restricted. Mucus pro- 
duction is to a large extent dependent on locomotory ac- 
tivity. Thus to describe the energetics of mucus production 
an understanding of movement patterns is also necessary. 
Limpet movement is complex but has been monitored ex- 
tensively (see LITTLE, 1989, and DELLA SANTINA & 
CHELAZZI, 1991, for reviews). Similarly, for any species 
where behavior differs widely and can place drains on 
assimilated energy, any single expression of energy allo- 
cation or flow should be viewed with caution. 

This study has demonstrated the intraspecific plasticity 
of an energetically important physiological process, pedal 
mucus production. This work suggests that before conclu- 
sions are drawn and extrapolations made from ecophysi- 
ological studies both temporal and spatial variation should 
be considered. 


ACKNOWLEDGMENTS 


Thanks to S. J. Hawkins and H. D. Jones for valuable 
discussion and guidance and to A. Taylor and L. H. Cook 


for criticism of the manuscript. This work was supported 
by the NERC, UK. 


LITERATURE CITED 


BALLANTINE, W. J. 1961. A biologically defined exposure scale 
for the comparative description of rocky shores. Field Studies 
1:1-19. 

CaLow, P. 1974. Some observations on locomotory strategies 
and their metabolic effects in two species of freshwater gas- 
tropods, Ancylus fluviatilis Mull. and Planorbis contortus Linn. 
Oecologia (Berlin) 16:149-161. 

Connor, V. M. 1986. The use of mucous trails by intertidal 
limpets to enhance food resources. Biological Bulletin 171: 
548-564. 

CULLEY, M. & K. SHERMAN. 1985. The effect of substrate 
particle size on the production of mucus in Haliotts tuberculata 
L. and the importance of this in a culture system. Aqua- 
culture 47:327-334. 

Davies, M.S. 1992. Heavy metals in seawater: effects on limpet 
pedal mucus production. Water Research 26:1691-1693. 

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THE VELIGER 


© CMS, Inc., 1993 
The Veliger 36(3):209-214 (July 1, 1993) 


Application of a ‘Two-Dimensional Electrophoresis 


Method to the Systematic Study of Notaspidea 


(Mollusca: Opisthobranchia) 
by 
RYOKO TSUBOKAWA!'! 
Tokyo University of Fisheries, Minato-ku, Tokyo, Japan 
AND 


JUN-ICHI MIYAZAKI 


Institute of Biological Sciences, The University of Tsukuba, Tsukuba-shi, Ibaraki 305, Japan 


Abstract. The phylogenetic relationships of four notaspidean opisthobranchs were examined using 
two-dimensional electrophoresis. The protein constituents of hearts were compared among five species 
belonging to four genera. The phylogeny deduced from the electrophoretic data supports the hypothesis 
of notaspidean phylogeny based on morphological and behavioral characters. To evaluate the validity 
of taxonomic ranks in the classification system proposed by Willan, the similarity values between 
notaspideans were compared with those obtained previously by two-dimensional electrophoresis on other 
animal groups. There is equivalence in electrophoretic distance at the level of genus between notaspideans 


and other animal groups. 


INTRODUCTION 


The Notaspidea is an order of opisthobranch mollusks 
characterized by a single gill situated on the right side of 
the body. WILLAN (1987) has established a new classifi- 
cation system of Notaspidea (Table 1) based upon an ex- 
amination of 57 morphological and behavioral qualitative 
characters. In his study he presented a cladogram derived 
by Hennigian methodology and a computer-generated 
phenogram of 11 notaspidean genera, which are fully con- 
gruent with each other. Despite this clarification at higher 
levels, some confusion in the taxonomy of Japanese No- 
taspidea remained, mainly due to synonymy at the level 
of species. Recently, the senior author has proposed that 
Japanese notaspideans be classified into 10 species be- 
longing to seven genera (TSUBOKAWA, 1991). However, 
the phylogeny of these Japanese species has not been in- 
vestigated. 


' Present address: Department of Phototechnology, Photon 
Medical Research Center, Hamamatsu University School of 
Medicine, 3600 Handa-cho, Hamamatsu-shi, Shizuoka, 431-31 
Japan. 


Two-dimensional electrophoresis is a useful technique 
for analyzing comprehensively protein constituents of tis- 
sues and organs. Protein electrophoretic patterns are phe- 
notypic characters at the molecular level which reflect ge- 
netic differences between species more directly than 
morphological characters, though all genetic changes can- 
not always be detected by electrophoresis (NEI & 
CHAKRABORTY, 1973; NEI, 1987). Similarity and genetic 
distance values between species can be obtained by com- 
paring electrophoretic patterns and can be employed for 
constructing dendrograms (AQUADRO & AVISE, 1981). The 
electrophoretic method has been applied in our serial stud- 
ies to investigate phylogenetic relationships of animals 
(MIYAZAKI et al., 1987, 1988), showing the usefulness of 
this method for phylogenetic analysis. In the Notaspidea, 
phylogenetic analysis at the molecular level has never been 
carried out. Therefore, application of two-dimensional 
electrophoresis to the systematic study of Japanese nota- 
spideans is likely to yield new information on genetic dif- 
ference and to deduce their phylogeny. Furthermore, it 
also permits us to evaluate Willan’s phylogenetic hypoth- 
esis on the basis of molecular data. 

In this study, two-dimensional electrophoresis is applied 


Page 210 


Table 1 


Classification of the order Notaspidea 
according to WILLAN (1987). 


Order Notaspidea Fischer, 1883 
Suborder Umbraculacea Dall, 1889 
Superfamily Tylodinoidea Gray, 1847 
Family Tylodinidae Gray, 1847 
Genus 7ylodina Rafinesque, 1819 
Genus Anidolyta Willan, 1987 
Family Umbraculidae Dall, 1889 
Genus Umbraculum Schumacher, 1817 
Suborder Pleurobranchacea Férussac, 1822 
Superfamily Pleurobranchoidea Férussac, 1822 
Family Pleurobranchidae Feérussac, 1822 
Subfamily Pleurobranchinae Feérussac, 1822 
Tribe Pleurobranchini Férussac, 1822 
Genus Pleurobranchus Cuvier, 1805 
Tribe Berthellini Burn, 1962 
Genus Berthella Blainville, 1825 
Genus Bathyberthella Willan, 1983 
Genus Pleurehdera Er. Marcus & Ev. Marcus, 1970 
Genus Berthellina Gardiner, 1936 
Subfamily Pleurobranchaeinae Pilsbry, 1896 
Genus Pleurobranchella Thiele, 1925 
Genus Pleurobranchaea Meckel in Leue, 1813 
Genus Euselenops Pilsbry, 1896 


to the systematic study of Japanese Notaspidea. Pairwise 
comparisons of electrophoretic patterns are carried out 
among five species belonging to four different genera. Sim- 
ilarity and genetic distance values are used to construct 
phylogenetic relationships of these species and the validity 
of WILLAN’s (1987) phylogenetic hypothesis is discussed. 
The similarity values between notaspideans are compared 
with those obtained previously on other animal groups to 
evaluate taxonomic ranks in Willan’s classification system. 


MATERIALS anp METHODS 
Samples 


Five species of Japanese notaspidean opisthobranchs, 
belonging to four different genera, were used for pairwise 
comparisons. Other members of the order are rare in Jap- 
anese waters, and were not available for the present study. 
The combination of each pair and the locality of each 
animal are as follows: 


(1) Pleurobranchus semperi (Wayssiére) from Onna, Oki- 
nawa Island versus Umbraculum sinicum (Gmelin) from 
O-shima Island, Izu Islands. 

(2) Berthellina citrina (Ruppell & Leuckart) from Susaki, 
Izu Peninsula versus Umbraculum sinicum from Su- 
saki, Izu Peninsula. 

(3) Pleurobranchaea japonica Thiele from off Miura Pen- 


The Veliger, Vol. 36, No. 3 


insula versus Umbraculum sinicum from Susaki, Izu 
Peninsula. 

Berthellina citrina from Susaki, Izu Peninsula versus 
Pleurobranchaea japonica from off Miura Peninsula. 

Pleurobranchus semper: from Onna, Okinawa Island 
versus Pleurobranchaea japonica from off Miura Pen- 
insula. 

Pleurobranchus semper: from Onna, Okinawa Island 
versus Berthellina citrina from Susaki, Izu Peninsula 
and from Kenzaki, Miura Peninsula. 

Pleurobranchus semperi from Aka-jima Island, Kerama 
Islands versus Pleurobranchus hirasei from Ryagi-jima, 
Izu Peninsula. 


(4 


WV 


(5 


WY 


(6 


wa 


(7 


a 


(8 


WH 


Umbraculum sinicum from Susaki, Izu Peninsula ver- 
sus the same species from Ir6-zaki, Izu Peninsula. 
Pleurobranchus semperi from Onna, Okinawa Island 
versus the same species from Aka-jima Island, Kerama 
Islands. 


(9 


EF 


In WILLAN’s (1987) classification system (Table 1), Um- 
braculum belongs to the family Umbraculidae of the sub- 
order Umbraculacea, one of the two suborders of the order 
Notaspidea. Pleurobranchus and Berthellina belong to the 
subfamily Pleurobranchinae of the family Pleurobranchi- 
dae of the other suborder Pleurobranchacea. Pleurobran- 
chaea belongs to the subfamily Pleurobranchaeinae of the 
family Pleurobranchidae. 


Electrophoresis 


Two-dimensional electrophoresis was carried out as de- 
scribed in HIRABAYASHI (1981), HIRABAYASHI et al. (1983), 
and OH-ISHI & HIRABAYASHI (1988). 

After narcotizing the animal, organs were dissected out 
in seawater, chilled on ice, and rinsed in filtered seawater 
to remove the blood. Then they were stored frozen at 
—80°C until use. Organs were homogenized with a Dounce 
homogenizer in 20 volumes of an extraction medium, which 
contained 8 M guanidine-HCl, 10% (6-mercaptoethanol, 
and 0.1 M Tris-HCl at pH 7.5. The homogenate was 
dialyzed for 3.5 hr against three changes of 5 M urea, 1 
M thiourea, and 0.16% $-mercaptoethanol at O0°C, and 
centrifuged at 40,000 rpm for 20 min with a Beckman 
TLA-100.3 rotor. The supernatant (40-100 uL) was sub- 
jected to first dimension isoelectric focusing with 1% aga- 
rose gel for 14,000 V-hr at 4°C. After isoelectric focusing, 
proteins in the agarose gel were fixed in a solution con- 
sisting of 10% trichloroacetic acid and 5% sulfosalicylic 
acid. The second dimension SDS-polyacrylamide gel elec- 
trophoresis, with a concentration gradient of acrylamide 
(12-20%), was carried out fundamentally according to 
LAEMMLI (1970). The proteins were stained with Coom- 
assie brilliant blue (STEPHANO et al., 1986). 

Preliminary electrophoresis was conducted on several 
organs of Plewrobranchaea japonica such as heart, foot mus- 
culature, and esophagus to determine the total number of 
protein spots in each electrophoretic pattern. The heart 


R. Tsubokawa & J.-I. Miyazaki, 1993 


Table 2 


Similarity and genetic distance among Japanese notaspi- 

deans. Similarity (F) and genetic distance (D) were cal- 

culated according to AQUADRO & AVISE (1981). Similarity, 

F = 2N,,/(N, + N,); Genetic distance, D = 1 — F. N,, 

is the number of spots shared by members x and y in each 

pair, and N, and N, are the numbers of spots scored for 
x and y, respectively. 


N,, 
Combination ND ING Ie D 

1 Pleurobranchus semper vs. 

Umbraculum sinicum 185 27 0.146 0.854 
2 Berthellina citrina vs. 

Umbraculum sinicum Wil 39) 102205 105780 
3 Pleurobranchaea japonica vs. 

Umbraculum sinicum 262 65 0.248 0.752 
4 Berthellina citrina vs. 

Pleurobranchaea japonica 295 S260 27.9 ON 21 
5 Pleurobranchus semperi vs. 

Pleurobranchaea japonica 182 53) 10:2910 105709 
6 Pleurobranchus semper vs. 

Berthellina citrina 256 81 6.316 0.684 
7 Pleurobranchus semper vs. 

Pleurobranchus hiraset LOZ ASOlE29N OSA 
8 Umbraculum sinicum vs. 

Umbraculum sinicum 270 262 0.970 0.030 
9 Pleurobranchus semperi vs. 

Pleurobranchus sempert 184 180 0.978 0.022 


protein had more than 100 spots that were suitable for 
comparison of protein constituents, and thus the heart was 
used in this study. 


Analysis 


To compare the two-dimensional electrophoretic pat- 
terns, the triplet method (MIYAZAKI et al., 1987) was used. 
The two samples to be compared plus their mixture were 
focused and electrophoresed at the same time. The elec- 
trophoretic patterns were photographed and compared vi- 
sually. Overlapping of protein spots from different samples 
were checked against the pattern of their mixture. For 
correct scoring of overlapping protein spots, varying vol- 
umes of supernatants were subjected to two-dimensional 
electrophoresis for each combination. Similarity was cal- 
culated according to the formula F = 2Nxy/(Nx + Ny), 
where F is the similarity between members x and y in 
each pair, Nxy is the number of protein spots shared by 
x and y, and Nx and Ny are the total numbers of protein 
spots scored for x and y, respectively (AQUADRO & AVISE, 
1981). The genetic distance (D) was given by the formula 
1D) = jl =" 18, 

The genetic distance values of interspecific combinations 
(1 to 6 in Table 2) were used to construct dendrograms 
with the unweighted pair-group method using the arith- 
meric average (UPGMA) (SOKAL & MICHENER, 1958) 


Page 211 
SS 
== =e goes > 


Br = 
| ; 


< 


—e 


Figure 1 


Typical two-dimensional electrophoretic patterns. Electropho- 
resis was carried out as described in the Materials and Methods 
section. The acidic end of the isoelectric focusing gel is to the 
right. The triplet method was used for comparison of protein 
constituents between two species. Patterns of heart proteins from 
Pleurobranchus semperi (A) and Pleurobranchaea japonica (C) and 
their mixture pattern (B) are shown here. 


and modified Farris method (TATENO et al., 1982) re- 
spectively. Because so few Pleurobranchus hirasei were ob- 
tained, this species was used only for obtaining the genetic 
distance of the congeneric combinations. 


RESULTS 


Typical two-dimensional electrophoresis patterns of hearts 
are shown in Figure 1. The total number of scored spots 
and the number of spots shared by each pair are repre- 
sented in Table 2. The similarity and the genetic distance 
of the nine pairs are also represented in Table 2. 


Page 212 


0.000 0.200 0.400 


The Veliger, Vol. 36, No. 3 


0.600 0.800 1.000 


Figure 2 


Distribution of the similarity values between Japanese notaspideans. The number corresponds with the pair number 


in Table 2. 


Figure 2 represents a distribution of the similarity values 
of the nine pairs. According to WILLAN’s (1987) classifi- 
cation system (Table 1), the values were assigned to con- 
specific populations (8 and 9), congeneric species (7), con- 
subfamilial genera (6), confamilial subfamilies (4 and 5), 
or different suborders (1, 2, and 3). The similarity values 
between conspecific populations were very high (8, F = 
0.970; 9, F = 0.978). On the other hand, those between 
consubfamilial genera (6, F = 0.316), confamilial subfam- 
ilies (4, F = 0.279; 5, F = 0.291), and different suborders 
(1, F = 0.146; 2, F = 0.220; 3, F = 0.248) were very low. 
The similarity value between congeneric species (7, F = 
0.629) took a middle position between the above values 
(8-9 vs. 1-6). The order of the similarity values corre- 
sponded well with the order of the taxonomic ranks. 


0.342 


Pleurobranchus semperi 


Berthellina citrina 


Pleurobranchaea japonica 


Umbraculum sinicum 


io 
© G 
B R x S * & 
y § ee oc ¢ & § S 
») « & O NY & A R 
Xi ¥ Cs we ¥ < © ss & Oo 
& J OS eS a SIS & 
& R s OS & e e & & } 
Figure 3 


A. Phenogram of four notaspidean species belonging to different 
genera. The phenogram was constructed by UPGMA using the 
genetic distance values represented in Table 2. B. Cladogram of 
11 notaspidean genera according to WILLAN (1987). Genera con- 
nected by heavy branches were used in this study. 


The phenogram of four species belonging to different 
genera, Pleurobranchus sempert, Berthellina citrina, Pleu- 
robranchaea japonica, and Umbraculum sinicum, was con- 
structed by UPGMA (SoKAL & MICHENER, 1958) and is 
represented in Figure 3. The phenogram suggests that the 
ancestor of U. sinicum was the first to diverge from the 
common ancestor of the three other species, and next the 
ancestor of Pleurobranchaea japonica branched off from the 
common ancestor of the remaining two species. However, 
the two nodes of branches leading to the latter three species 
(Figure 3A, a and b) were situated very close to each other. 

The UPGMA phenogram is based on the unverifiable 
assumption that evolutionary rates of organisms are uni- 
form. Therefore, the modified Farris method (TATENO et 
al., 1982) was used to construct the network and the rooted 
tree shown in Figure 4. The root was situated at the middle 
point of the longest branch connecting Berthellina citrina 
and Umbraculum sinicum. The modified Farris method 
does not rely on the assumption of uniformity of evolu- 
tionary rate, but the above rooting of the tree equates 
evolutionary rates of the lines leading to the two species. 
Another rooting method places the root on the branch 
connecting outgroup and ingroup clusters. Of the four 
species examined in this study, U. sinicum has been chosen 
as the outgroup, because the Umbraculacea (including the 
genus Umbraculum) have been separated consistently from 
other groups of Notaspidea (BURN, 1962; THOMPSON, 1976) 
because of their unique characters, including an external 
shell, two pairs of tentacles on an oral veil, the gill orig- 
inating from the left anterolateral portion of the body, a 
ring-shaped thin jaw membrane in the buccal mass, and 
a unique internal and external reproductive system (WIL- 
LAN, 1987; TSUBOKAWA, 1991). When U. sinicum was 
treated as an outgroup, the tree was rooted between U. 
stnicum and node b, which connects the line leading to 
Pleurobranchus semperi and B. citrina and the line to Pleu- 
robranchaea japonica. The tree is substantially consistent 
with the midpoint-rooted tree. The rooted tree (Figure 4B) 
also gave the same topology as that of the UPGMA tree 
(Figure 3A), though there were slight differences in branch 
length. 


DISCUSSION 


AQUADRO & AVISE (1981) have shown that genetic distance 
ranks obtained by two-dimensional electrophoresis are 
highly concordant with taxonomic levels in rodent species. 


R. Tsubokawa & J.-I. Miyazaki, 1993 


Page 213 


A Pleurobranchus 
semperi 


Pleurobranchaea 
Japonica 


Berthellina 


citrina 
Umbraculum 
sinicum 
0.336 Pleurobranchus semperi 
0.032 a 
Berthellina citrina 
0.015 b 


Pleurobranchaea japonica 


Umbraculum sinicum 


Figure 4 


Unrooted network and rooted tree of four notaspidean species. 
The network (A) and tree (B) were constructed by the modified 
Farris method using the genetic distance values. The rooted tree 
was constructed by situating a root at the middle point of the 
longest branch of the network. 


Furthermore, MIYAZAKI et al. (1987) have suggested that 
two-dimensional electrophoresis provides a valuable tool 
for systematics in estimating and evaluating genetic dis- 
tances. As shown in Table 2 and Figure 2, the order of 
the similarity values of nine pairs corresponded with that 
of the taxonomic ranks based on WILLAN’s (1987) clas- 
sification system (Table 1). Therefore, the present results 
show that two-dimensional electrophoresis is a useful tech- 
nique for examining phylogenetic relationships of Nota- 
spidea, confirming the conclusions of previous studies. 
When the similarity values for the Notaspidea are com- 
pared with those obtained by two-dimensional electropho- 
resis on animals of other groups (AQUADRO & AVISE, 1981; 
MIvAzakKi et al., 1987, 1988), the values in the correspond- 
ing taxonomic combinations were similar between nota- 
spideans and other animal groups (Table 3). Therefore, 
taxonomic ranks in WILLAN’s (1987) classification system 
are supported by electrophoretic data. However, the values 
between notaspidean confamilial genera (4, 5, and 6 in 
Table 2) and conordinal families (1, 2, and 3 in Table 2) 
were low, when compared with those of rodents. A possible 
explanation for such differences is that ranks in rodents 


Table 3 


Comparison of the similarity values among four different 
animal groups. The similarity values are arranged in the 
corresponding taxonomic combinations. 


Horse- 
shoe 
crab 
Rodent cardiac 

liver muscle Nota- 
(Aqua- (Mlya- Land snail spidea 
DRO & ZAKI whole body heart 
Taxonomic  AVISE, et al., (MIYAZAKI (this 
combination 1981) 1987) et al., 1988) study) 
Conspecific 0.951 0.989 0.978 
population 0.916 0.913 0.970 
Congeneric 0.852 0.649 0.878 0.795 0.629 

species 0.812 0.639 0.846 0.768 

0.639 0.834 0.766 

0.833 0.736 

0.824 0.667 
Confamilial 0.599 0.371 0.316 
genus 0.547 0.320 0.291 
0.309 0.279 
Conordinal 0.504 0.248 
family 0.220 


0.146 


and notaspideans are not equal. This indicates that diver- 
gence time between these notaspidean species is longer than 
that between rodent species in the corresponding taxonom- 
ic combination above subfamily, although the same taxo- 
nomic rank should ideally reflect the same evolutionary 
time in all phylogenetic lines. To formulate such an ideal 
and authentic classification system throughout the biolog- 
ical world, it is necessary to know absolute evolutionary 
time or relative evolutionary time. Practically, genetic dis- 
tance data at the molecular level are available, because 
they reflect relative evolutionary time. Therefore, more 
comprehensive studies using several other methods are re- 
quired to give accurate genetic distance measures. In the 
latter case, although there is no evidence which supports 
differences in evolutionary rates of proteins between no- 
taspideans and rodents, the possibility cannot be excluded. 

Two trees of four notaspidean genera (Figure 3A, 4B), 
which were depicted using the UPGMA and the modified 
Farris method with the present genetic distance data, gave 
the same topology. The topology is consistent with that of 
WILLAN’s (1987) cladogram (Figure 3B), which was con- 
structed on morphological and behavioral characters using 
Hennigian methodology. Agreement among the three trees 
strongly suggests reliability of the phylogenetic relation- 
ships of the four genera. However, only small differences 
were found in the similarity values of pairs 1 to 6 (Table 
2), making the positions of three nodes (Figures 3A and 
4B, a, b, and c) of the trees very close to each other. This 
may be ascribed to two causes. One is the high sensitivity 


Page 214 


The Veliger, Vol. 36, No. 3 


of two-dimensional electrophoresis for detecting differ- 
ences in protein constituents. Therefore, protein differ- 
ences between notaspideans, which can be detected by this 
method, approach a saturation level. The second is the 
separation of the ancestral taxa at almost the same time 
geologically. In either case, we must be careful to conclude 
that the phylogenetic relationships of the four genera are 
definitive, because differences in the similarity values were 
small, taking account of probable deviations of evolution- 
ary changes at the molecular level. Therefore, further ac- 
cumulation of phylogenetic information obtained by using 
other approaches is required to test the existing notaspi- 
dean phylogenetic hypothesis. 


ACKNOWLEDGMENTS 


We are most thankful to Prof. K. Kuwasawa (Tokyo Met- 
ropolitan University), Mr. H. Ueda, Mr. Y. Tsuchiya, 
Mr. T. Sato, and Dr. T. Hirata (The University of Tsu- 
kuba), Dr. A. Kakuno, Mr. K. Shimoike, and Mr. T. 
Hayashibara for providing us with the specimens used for 
this investigation. We are much indebted to Prof. T. Hira- 
bayashi (The University of Tsukuba) for his helpful advice 
on electrophoretic techniques and Dr. R. C. Willan 
(Northern Territory Museum, Darwin, Australia) for as- 
sistance in revising the manuscript. We are also thankful 
to Prof. T. Okutani (Tokyo University of Fisheries) for 
useful criticism and encouragement. 


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Molecular Evolution 2:323-328. 

Ou-IsHI, M. & T. HIRABAYASHI. 1988. Micro two-dimensional 
gel electrophoresis with agarose gel in the first dimension. 
The Physico-Chemical Biology 32(3):113-120. 

SOKAL, R. R. & C. D. MICHENER. 1958. A statistical method 
for evaluating systematic relationships. The University of 
Kansas Science Bulletin 38(2):1409-1438. 

STEPHANO, J. L., M. GouLpD & L. Rojas-GALicia. 1986. Ad- 
vantages of picrate fixation for staining polypeptides in poly- 
acrylamide gels. Analytical Biochemistry 152:308-313. 

TATENO, Y.,M. NEI & F. TAJIMA. 1982. Accuracy of estimated 
phylogenetic trees from molecular data. I. Distantly related 
species. Journal of Molecular Evolution 18:387-404. 

TuHompson, T. E. 1976. Biology of Opisthobranch Molluscs. 
Vol. 1. The Ray Society: London. 

TsuBOKAWA, R. 1991. Taxonomic and phylogenetic study on 
Notaspidea in Japan (Mollusca, Opisthobranchia). Doctoral 
Dissertation, Tokyo University of Fisheries, Tokyo. 

WILLAN, R. C. 1987. Phylogenetic systematics of the Nota- 
spidea (Opisthobranchia) with reappraisal of families and 
genera. American Malacological Bulletin 5(2):215-241. 


The Veliger 36(3):215-219 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Karyotype and Nucleolus Organizer Regions in 


Ostrea puelchana (Bivalvia: Ostreidae) 


by 


ANA INSUA anp CATHERINE THIRIOT-QUIEVREUX'! 


Observatoire Océanologique, Université P. et M. Curie—CNRS-INSU, 
BP 28, 06230 Villefranche-sur-Mer, France 


Abstract. 


The chromosomes of the Argentinian oyster, Ostrea puelchana, were studied using karyomet- 


ric analysis after conventional Giemsa staining, and silver-staining. The karyotype consists of 4 meta- 
centric, five submetacentric, and one small telocentric chromosome pairs. The silver-stained nucleolus 
organizer regions (NORs) were terminally located on the short arms of the submetacentric pairs 2 and 
4. A variable number of one to three Ag- NOR chromosomes were found within and between animals, 
revealing a heteromorphism in the number of active NOR sites per cell. The most frequent case was 
one Ag-NOR chromosome in pairs 2 and 4 simultaneously. Comparative analysis of the karyotypes of 
O. puelchana, O. edulis, and O. denselamellosa supports the taxonomic subdivision of the genus Ostrea 


into two subgenera. 


INTRODUCTION 


Chromosomes of Ostreacea have been studied in 24 species 
of four genera in Ostreidae and two genera of Pycnodon- 
teidae (see VITTURI et al., 1985, and IEYAMA, 1990, for 
literature). Many oysters have the same chromosome num- 
ber, 2n = 20, and their karyotypes consist of only meta- 
centric and submetacentric chromosomes. But as investi- 
gated species increase, different chromosome numbers (2n 
= 18) have been observed (IEYAMA, 1990) as well as karyo- 
types with subtelocentric or telocentric chromosomes 
(THIRIOT-QUIEVREUX, 1984; VITTURI et al., 1985; IEYAMA, 
1990). Interspecific chromosomal differences in Ostreacea 
consist mainly of different proportions of morphological 
chromosome types. But studies of the nucleolus organizer 
regions (NORs) have also shown interspecific differences 
(THIRIOT-QUIEVREUX & INSUA, 1992). 

According to HARRY (1985), the genus Ostrea Linné, 
1758, includes two subgenera, Ostrea s.s., which includes 
Ostrea (Ostrea) edulis Linné, 1758, and Ostrea (Ostrea) 
denselamellosa Lischke, 1869, and Eostrea Ihering, 1907, 
with Ostrea (Eostrea) puelchana D’Orbigny, 1841. 

Karyotypes and NORs were previously studied in Ostrea 
edulis (THIRIOT-QUIEVREUX, 1984; THIRIOT-QUIEVREUX 
& Insua, 1992) and in O. denselamellosa (INSUA & THIRIOT- 
QUIEVREUX, 1991). These two species are karyologically 


''To whom correspondence should be sent. 


distinguished by different proportions of metacentric chro- 
mosomes and by the different locations of the NORs in 
the karyotypes. 

In the present paper, the karyotype and NORs were 
studied in Ostrea (Eostrea) puelchana in order to analyze 
cytotaxonomical relationships within the genus Ostrea. 


MATERIAL anD METHODS 


Specimens came from the experimental rearing of Argen- 
tinian Ostrea puelchana carried out in IFREMER French 
oyster farming site. 

Oysters from 3 to 4 cm were incubated for 8 hr with 
0.005% colchicine in seawater. The gills were then dis- 
sected and treated for 30 min in 0.9% sodium citrate in 
distilled water. The material was then fixed in a freshly 
prepared solution of absolute alcohol and acetic acid (3:1) 
with three changes of 20 min duration. Each slide prep- 
aration was made from one individual oyster using an air- 
drying technique (THIRIOT-QUIEVREUX & AYRAUD, 1982). 
For conventional karyotypes, slides were stained directly 
with Giemsa (4%, pH 6.8) for 10 min. Photographs of 
suitable mitotic metaphases were taken with a Zeiss III 
photomicroscope, and after karyotyping, chromosome 
measurements of 10 cells in mitotic metaphase were made 
with a digitizer (Summa Sketch II) interfaced with a Mac- 
intosh Classic. Data analysis was performed with the Excel 
macro program. Terminology relating to centromere po- 
sition follows that of LEVAN et al. (1964). 


Page 216 The Veliger, Vol. 36, No. 3 


Table 1 


Chromosome measurements and classification derived from 10 metaphase cells of Ostrea puelchana. 


Relative length Arm ratio Centromeric index 


Chromosome = EEE ee ee ee Classitie 
pair no. Mean SD Mean SD Mean SD cation 

1 131957 0.702 0.818 0.047 44.776 1.428 m 

2 12.287 0.803 0.548 0.043 35.196 1.754 sm 
3 11.610 0.551 0.832 0.093 45.223 avo! m 

4 11135 0.602 0.478 0.044 32.171 1.969 sm 
5 10.339 0.409 0.474 0.055 31.889 2.461 sm 
6 10.012 0.274 0.775 0.071 43.487 2.256 m 

il 9.081 0.650 0.358 0.031 26.157 1.615 sm 
8 8.274 0.643 0.805 0.071 44.442 2.134 m 

9 8.111 0.371 0.521 0.068 34.000 3.085 sm 
10 5.194 0.361 0.058 0.015 5.387 1.354 t 


1 2 3 4 5 
é 
6 Yi 8 9 10 
a ° a 
. 
] 2 3 4 5 
* ” 
& 
6 7 8 9 10 
B —_———_ 
Figure 1 


Karyotypes of Ostrea puelchana. A. Conventional Giemsa staining. B. Silver-staining. Note one chromosome with 
Ag-NORs in chromosome pairs 2 and 4. 


A. Insua & C. Thiriot-Quievreux, 1993 


Relative length 


Page 217 


4 5 7 9 10 


Chromosome pairs 


Figure 2 


Ideogram constructed from relative length and centromeric index values in Ostrea puelchana. 


The NORs were silver-stained either directly on un- 
stained slides using the technique of HOWELL & BLACK 
(1980), modified by GOLD & ELLISON (1982), or on Giem- 
sa-stained slides followed by destaining with alcohol. 


RESULTS 


A diploid complement of 2n = 20 was found in 70 mitotic 
metaphases from 13 animals. Nine animals were randomly 
selected and a total of 263 metaphases were scored for 
chromosome counts. The percentage of aneuploid cells (2n 
= 17, 18, or 19) was 10.65%. 

For karyotyping, the chromosomes of 22 well-spread 
metaphase plates were cut out from photomicrographs and 
paired on the basis of size and centromere position. Chro- 


100% 


0 1 2 
pair 2 


mosome measurements were taken from the 10 best spreads 
and the means and SD of relative length (100 x absolute 
chromosome pair length/total length of haploid comple- 
ment), arm ratio (length of short arm/length of long arm) 
and centromere index (100 x length of short arm/total 
length of chromosome) together with the chromosome clas- 
sification are given in Table 1. The karyotype (Figure 1A) 
consists of 10 chromosome pairs of sharply decreasing size. 
The last pair is strikingly smaller than the others. Pairs 
1, 3, 6, and 8 are metacentric. Pairs 2, 4,5, 7, and 9 are 
submetacentric and pair 10 is telocentric (Figure 2). 

The NORs were examined in 106 metaphase plates 
derived either from slide preparations silver-stained di- 
rectly or from preparations silver stained after Giemsa 
staining. A variable number of one to three Ag- NOR chro- 


0 1 2 
pair 4 


Figure 3 


Proportions among cells showing one, two, or zero active NORs after the analysis of 106 metaphase cells in 


chromosome pairs 2 and 4. 


Page 218 


Centromeric index 


37.5 | 


The Veliger, Vol. 36, No. 3 


25 - 
st 8 
10 
12.5 
t 
& 
0 
5 6 7 8 10 11 12 13 14 
Relative length 
Figure 4 


Comparison of morphology and size of the different chromosome pairs in Ostrea puelchana (open square), O. edulis 
(black square), and O. denselamellosa (open circle). Asterisk indicates Ag-NOR chromosome pair. 


mosomes was identified within and between individuals. 
In all cases, the chromosomal position of the Ag- NOR was 
found to be terminal on the short arms of the submeta- 
centric pairs 2 and 4. The two homologous chromosomes 
of these pairs showed heteromorphism involving apparent 
NOR activity. Figure 3 gives the proportions among cells 
showing one, two, or zero active NORs in chromosome 
pairs 2 and 4. The most frequent case (41.51%) was one 
silver-stained NOR chromosome, simultaneously in pairs 
2 and 4. 


DISCUSSION 


The diploid number of 2n = 20 observed in Ostrea puel- 
chana is common among Ostreacea. The percentage of 
aneuploid cells scored here is close to that recorded in other 
ostreid species (THIRIOT-QUIEVREUX, 1986; INSUA & 
‘THIRIOT-QUIEVREUX, 1991). 

Comparison of morphometric measurements of chro- 
mosomes in Ostrea puelchana (this paper), O. denselamellosa 
(INSUA & ‘THIRIOT-QUIEVREUX, 1991), and O. edulis 
(THIRIOT-QUIEVREUX, 1984, table 3) is given in Figure 
4. Among these three species, three chromosome pairs (1, 
3, and 9) share the same position and the same morphology 
in the karyotypes. The other pairs overlap two categories 
of the chromosome classification. Pair 10 is strikingly dif- 
ferent among these three species (metacentric in O. edulis, 
submetacentric in O. denselamellosa, and telocentric in O. 
puelchana). Thus, O. puelchana differs from O. denselamel- 
losa and O. edulis by the different proportions of metacen- 
tric and submetacentric chromosome pairs, and especially 
by the occurrence of a small telocentric pair. 

Comparison of the pattern of Ag-NORs in Ostrea puel- 


chana (this paper), O. denselamellosa (INSUA & THIRIOT- 
QUIEVREUX, 1991), and O. edulis (THIRIOT-QUIEVREUX 
& InsuA, 1992) indicates that (i) the chromosomal location 
of NORs was different in the three species: terminal on 
the short arm of submetacentrics in O. puelchana, terminal 
on metacentrics in O. denselamellosa and terminal on the 
long arm of submetacentrics in O. edulis, (11) the position 
of NORs within karyotypes showed a specific pattern: 
pairs 2 and 4 in O. puelchana, pairs 3 and 8 in O. dense- 
lamellosa and pairs 9 and 10 in O. edulis, allowing iden- 
tification of chromosomal differences in the morphologi- 
cally similar pairs 3 and 9, and finally, (iii) heteromorphism 
involving the apparent NOR activity occurred in the three 
species. 

In conclusion, the karyotype and NOR pattern of Ostrea 
puelchana clearly separate this species from the two other 
Ostrea species previously examined, perhaps giving cyto- 
taxonomic arguments for the Ostrea subdivision (HARRY, 
1985) into two subgenera, Ostrea s.s. and Eostrea. 


ACKNOWLEDGMENTS 


This work was supported by the CNRS (EP 17). We are 
grateful to A. G. Martin (IFREMER, La Trinité sur- 
Mer, France) for providing Ostrea puelchana animals. We 
thank P. Chang for corrections in English and G. Quélart 
for her excellent technical assistance. 


LITERATURE CITED 


Go.p, J. R. & J. R. ELLIson. 1982. Silver staining for nu- 
cleolar organizing regions of vertebrate chromosomes. Stain 
Technology 58:51-55. 


A. Insua & C. Thiriot-Quiévreux, 1993 


Harry, H.W. 1985. Synopsis of the supraspecific classification 
of living oysters (Bivalvia: Gryphaeidae and Ostreidae). The 
Veliger 28:121-158. 

Howe.L_, W. M. & D. A. Biack. 1980. Controlled silver- 
staining of nucleolus organizer regions with a protective 
colloidal developer: a 1-step method. Experientia 36:1014- 
1015. 

IEYAMA, H. 1990. Chromosomes of the oysters, Hyotissa im- 
bricata and Dendostrea folium (Bivalvia: Pteriomorphia). Ve- 
nus (The Japanese Journal of Malacology) 49:63-68. 

Insua, A. & C. THIRIOT-QUIEVREUX. 1991. The characteriza- 
tion of Ostrea denselamellosa (Mollusca Bivalvia) chromo- 
somes: karyotype, constitutive heterochromatin and nucle- 
olus organizer regions. Aquaculture 97:317-325. 

LEVAN, A., K. FREDGA & A. A. SANDBERG. 1964. Nomencla- 
ture for centromere position in chromosomes. Hereditas 52: 
201-220. 


Page 219 


THIRIOT-QUIEVREUX, C. 1984. Analyse comparée des caryo- 
types d’Ostreidae (Bivalvia). Cahiers de Biologie Marine 25: 
407-418. 

THIRIOT-QUIEVREUX, C. 1986. Etude de l’aneuploidie dans 
différents naissains d’Ostreidae (Bivalvia). Genetica 70:225- 
231. 

THIRIOT-QUIEVREUX, C. & N. AYRAUD. 1982. Les caryotypes 
de quelques espéces de Bivalves et de Gastéropodes marins. 
Marine Biology 70:165-175. 

THIRIOT-QUIEVREUX, C. & A. INSuA. 1992. Nucleolar orga- 
nizer region variation in three oyster species. Journal of 
Experimental Marine Biology and Ecology 157:33-40. 

VITTURI, R., P. CARBONE & E. CATALANO. 1985. The chro- 
mosomes of Pycnodonta cochlear (Poli) (Mollusca, Pelecypo- 
da). Biologische Zentralblatt, Leipzig 104:177-182. 


The Veliger 36(3):220-227 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Variability in Growth and Age Structure Among 
Populations of Ribbed Mussels, 


Geukensia demissa (Dillwyn) (Bivalvia: Mytilidae), in 
Jamaica Bay, New York (Gateway NRA) 


by 


DAVID R. FRANZ 


Biology Department, Brooklyn College, City University of New York, 
Brooklyn, New York 11210, USA 


AND 


JOHN T. TANACREDI 


United States National Park Service, Gateway National Recreation Area, 
Brooklyn, New York 11234, USA 


Abstract. 


Growth rates, body weight, density and biomass of ribbed mussels, Geukensia demissa 


(Dillwyn), were determined at Spartina alterniflora marsh-flat sites in Jamaica Bay, New York (Lower 
Hudson Estuary). Cumulative growth and annual growth increments varied but rates were lower at 
sites within the central bay relative to peripheral sites. Local variability both in size at Ring-1 and size- 
specific annual growth rates probably account for the variability in cumulative length. No patterns were 
noted in frequency distributions of shell size but congruence in age structure was observed among 
neighboring sites in some areas of the bay. Length-specific dry body weights were lower in the central 
bay. Mussel densities were greater within Jamaica Bay than at most other locations reported in the 
literature and estimated biomass values were lower. Growth rates of Jamaica Bay mussels were lower 
than other populations in the northeastern American coast. Four hypotheses that may account for 
observed Geukensia growth rates in Jamaica Bay are presented and discussed: higher population density, 
higher vertical marsh levels, variability in phytoplankton quality and/or quantity, long-term sublethal 


chemical pollution. 


INTRODUCTION 


Jamaica Bay is an urban estuary located at the south- 
western end of Long Island and comprises the easternmost 
component of the Lower Hudson River estuarine system. 
Bounded on the north by the New York City boroughs of 
Brooklyn and Queens, and on the east by Long Island’s 
Nassau County, most of the bay at present is included 
within the Gateway National Recreation Area. In spite of 
severe human impacts from pollution, development, and 
population pressure, Jamaica Bay remains a critical local 
resource for migrating shorebirds and waterfowl and pro- 
vides nesting sites for several endangered wildlife species. 


The intertidal zone of much of Jamaica Bay is bordered 
by Spartina salt marshes. A ubiquitous inhabitant of this 
community is the Atlantic ribbed mussel, Geukensia de- 
missa (Dillwyn, 1817) (BERTNESS, 1984). This bivalve may 
prove useful as a candidate for long-term monitoring of 
environmental quality in Jamaica Bay. Its advantages in- 
clude: (1) Mussels are relatively long-lived (>10 yr at 
many places) and moderately large (>1 g dry weight); (2) 
Mussels are relatively immobile (after a post-settlement 
period of active movement) and accessible year round; (3) 
The age of individual mussels can be determined by enu- 
meration of external annuli (LUTZ & CasTaGna, 1980; 
BROUSSEAU, 1984); and (4) As long-lived filter feeders, 


D. R. Franz & J. T. Tanacredi, 1993 Page 221 
ie iS QUEENS 
BROOKLYN © . We. KY: | 
eS ue oo E a at an oe M “3 Be 35: 
OB . x A foot - ey Sie NOD 
oN JAMAICA ~: ican | Pe 
oe We \ Fs Sr ae ee 
(RA ‘& : 
J 7 NASSAUL”” 
Xi FLOYD: > BENNETT: 1 CO! & 
4 \ :coaTeway NRA). : ae 
ROCKAWAY 
INLET 
. 35’ 
: is ATLANTIC OCEAN 
56’ 52’ 48 44 


Figure 1 


Map of Jamaica Bay (New York City) showing location of mussel sampling sites. W, water; PB, Plum Beach; 
RA, Riding Academy; FC, Fresh Creek; BB, Black Bank; NC, North Channel; JO, Joco; In, Inwood; DR, Drucker; 


HQ, Headquarters; LEM, Inner Little Egg; OLE, Outer Little Egg. 


mussels may integrate the effects of low concentrations of 
suspended or dissolved toxic materials, which may be mea- 
surable as sublethal modifications of physiological func- 
tions such as growth or reproduction. The prerequisite for 
the use of mussels for this purpose is an adequate under- 
standing of their ecology, particularly the role of natural 
variables in affecting these physiological functions. The 
purposes of the research reported here were to determine 
the variability in Geukensia growth rates among sites with- 
in Jamaica Bay, and to compare growth with data from 
other locations. 


MATERIALS anp METHODS 
Study Sites 


Mussel populations (Figure 1) were selected to include 
a range of habitats within Jamaica Bay as well as a site 
just outside of the Bay proper (Plum Beach). At all sites, 
mean tidal range is close to 1.5 m. Sites were visited be- 
tween June and September 1991. At all locations, collec- 
tions came from the marsh flat, which is the section of the 
“tall” Spartina alterniflora salt marsh immediately upshore 
of the marsh edge, and characterized by the presence of 


Spartina culms. All marsh-flat samples were collected ap- 
proximately 1 m from the marsh edge. 


Analyses 


For analyses of growth, entire sections of turf containing 
mussels were cut by spade and brought to the laboratory, 
where larger mussels were removed by hand, and small 
mussels were washed into a 1-mm sieve. Barnacles and 
epiphytic growth were scraped from larger mussels, which 
were scrubbed with a metal brush. Mussels used for age 
determination were steamed open, the flesh was removed, 
and the paired valves were numbered. Age was determined 
by counting external growth annuli following the methods 
of Lurz & CasTAGNA (1980) and BROUSSEAU (1984). The 
growth annulus appears at the time of new growth begin- 
ning in May. Transmitted light was used to identify annuli 
in smaller mussels. Annuli were then confirmed by ex- 
amination of the outer shell surface under the dissecting 
microscope. Shells of larger, older mussels were soaked in 
Clorox to remove the periostracum. The shell length cor- 
responding to each annulus was measured with vernier 
calipers. 

Mussel density (m~*) was estimated at eight sites. Mus- 


Page 222 


MEAN SHELL LENGTH (MM) 


QO ter2) °3)4. SG 7 819) 10) ae: 13) 114) 15550 


RING NO. 


The Veliger, Vol. 36, No. 3 


NORTH CHANNEL 


JOCO 

MEAN 

LITTLE EGG 
RIDING ACADEMY 
BLACK BANK 
INWOOD 

200 
DRUCKER 

HQ 


PLUM BEACH 


PERCENT INCREASE 


100 


INITIAL LENGTH (MM) 


Figure 2 


A. Cumulative growth curves of nine mussel populations. B. Fitted size-specific relative growth curves. The y-axis 
is the log(mean percent annual length increase); x-axis is the initial length of a mussel at the beginning of a growth 
season. The curve labelled “mean” is generated using regression coefficients averaged for all populations, and may 
be considered as an average relative growth curve for Jamaica Bay mussels. 


sels were counted in 18 circular quadrats (area = 346 cm?) 
which were located randomly along a line stretched par- 
allel to the marsh edge. 

Dry body weight/shell length relationships were deter- 
mined for six populations in July 1991. For each popu- 
lation, 25 mussels spanning the available size range were 
selected. After measuring shell length, bodies including 
fluids were removed by dissection into pre-weighed pans. 
Tissues were dried at 70°C for 48 hr and re-weighed using 
a Metler Microbalance. Log-linear regressions of dry 
weight vs. shell length were used in conjunction with den- 
sity and size-frequency distributions of mussels to estimate 
biomass. 


RESULTS 
Cumulative and Relative Growth 


Cumulative growth curves for nine marsh-flat mussel 
populations from a range of sites within Jamaica Bay 


(Figure 2A) show that higher growth rates occurred at 
sites located away from the central core of the bay (e.g., 
Inwood, Little Egg Marsh, Plum Beach, and Riding Acad- 
emy). Lower growth occurred at sites within the central 
core of the bay (e.g., Drucker Marsh, North Channel 
Marsh and Black Bank Marsh). Mussel length at year-1 
was a poor predictor of size at age-8 (R? = 0.31, P = 0.07) 
but probably is a factor of importance in determining as- 
ymptotic future size. Another factor is the geographical 
position of the population within the bay. 

In order to distinguish between these factors, data from 
the growth curves in Figure 2A are rearranged in Figure 
2B as size-specific relative growth curves—z.e., the annual 
growth increment as a percentage of length at the initiation 
of growth for each year. These are fitted curves based on 
linear regressions of the log[(annual growth/initial length) 
x 100] vs. initial length. Initial length is the mean length 
of an age cohort at the start of any growing season; annual 
growth is the mean increment in length for the cohort by 


D. R. Franz & J. T. Tanacredi, 1993 


Page 223 


DEVIATION FROM PREDICTED MEAN LENGTH 


RING NO. 
Figure 3 


NORTH CHANNEL 
JOCO 

MEAN 

LITTLE EGG 
RIDING ACADEMY 
BLACK BANK 
INWOOD 
DRUCKER 


HQ 


Predicted growth curves for Jamaica Bay populations are generated using observed initial (Ring-1) mean lengths 
in combination with the “mean” growth coefficients for Jamaica Bay from Figure 2B. If the mean curve accurately 
portrays growth for Jamaica Bay mussels, observed and predicted growth curves would be identical. Note that 
observed growth tends to be lower than predicted at sites in the central bay but higher at sites distant from the 


central core and outside of the bay. 


the end of the growing season. Linear regression coefh- 
cients used to generate these curves and regression statistics 
are summarized in Table 1. An average growth curve for 
all populations (Figure 2B) has been used to reconstruct 
the cumulative growth curves. The average curve is based 
on the mean regression coefficients of all populations. These 
coefficients can then be used to simulate a cumulative growth 
curve for any site by using the observed mean year-1 length 
for that site as a starting point. To the extent that the 
average curve in Figure 2B accurately portrays a gener- 
alized growth strategy for Jamaica Bay mussel popula- 
tions, the resulting “predicted” growth curves should be 
equivalent to the observed curves. Deviations between the 
observed and predicted growth curves in relation to age 
are shown in Figure 3 for each site. 


Frequency Distributions of Size and Age 


Frequency distributions of age and shell length for all 
populations are shown in Figure 4. Shell-length distri- 
butions are polymodal and variable, with no pattern of 
similarity among sites. The absence of small mussels at 
sites such as North Channel and Inwood may indicate 
scarcity of 1991 and, possibly, 1990 year classes. 


Mussel Body Weights, Density, and Biomass 


Regression coefficients [log(dry weight, g) = a + b 
log(shell length, mm)] for six populations, and fitted curves 
reflecting these coefficients are shown in Table 1 and Fig- 
ure 5. Note that length-specific dry body weight (DW) is 
highest outside of Jamaica Bay (Plum Beach) and is lower 
at sites within the central core of the bay (Black Bank, 
Fresh Creek, Drucker). Mussel density at eight marsh- 
flat sites (Table 2) ranged between 600 and 1900 m~’. 

Estimates of biomass (g DW m_~’) for eight marsh-flat 
populations (Table 2) show that biomass ranged from 0.21 
kg (Drucker) up to 0.46 kg (Plum Beach). At sites within 
Jamaica Bay, biomass ranged from 0.21 to 0.42 kg. 


DISCUSSION 


Mussel populations in the central core of Jamaica Bay 
exhibit lower growth in comparison with more distant sites 
within the bay and with other locations in the northeastern 
American coast. This can be seen most clearly in the com- 
parison between observed relative growth curves and pre- 
dicted curves based on average growth statistics for all 
populations (Figure 3). Although the observed and pre- 


Page 224 


PLUM BEACH 


LITTLE EGG 


FRESH CREEK 


BLACK BANK 


Mth 


DRUCKER 


NO. MUSSELS 


13 5 7 9 11 13 


AGE (YEARS) 


The Veliger, Vol. 36, No. 3 


30-] PLUM BEACH 


FRESH CREEK 


BLACK BANK 


RIDING ACADEMY 


NORTH CHANNEL 


0 20 40 60 80 100 


LENGTH (MM) 


Figure 4 


Left panel shows age structure of each population (excluding 1991-class mussels). Right panel shows shell length- 
frequency distributions at all sites based on collections taken between June and September 1991. 


dicted curves are similar at some sites (HQ, Little Egg, 
Joco), the predicted curves deviate from the observed curves 
at others. If cumulative growth curves were determined 
primarily by size at year-1, then the pattern of deviation 
relative to geographical location should be random. How- 
ever, this clearly is not the case (Figure 3). At sites closer 
to the entrance to Jamaica Bay (Plum Beach, Riding Acad- 
emy) the observed growth curves exceed the predicted. At 
sites in the central bay (HQ, North Channel, Drucker, 
Black Bank) the observed growth is lower than the pre- 
dicted. Growth rates at the Inwood site are anomalously 


high. However, this population is located within the warm- 
water plume of an electric generating station. These data 
suggest that mussel populations in the central bay may be 
more stressed than populations located peripherally, as 
reflected by a smaller annual proportional allocation to 
growth—1.e., mussels of any given size in the central bay 
increase in size by a smaller percentage of starting size per 
year than other populations. 

Although no patterns in population size structure were 
discernible, there was congruence in age composition be- 
tween some sites. For example, all of the northern sites 


Dake Branzisc sil Wanacredi, 1993 


‘Table 1 


Regression statistics for Geukensia demissa. 


A. Regression statistics: log(annual length increment/initial 
length) vs. initial length. 


Site b a if 
North Channel —0.035 0.499 0.83 
Little Egg —0.026 0.473 0.94 
Black Bank —0.034 0.532 0.97 
Drucker —0.032 0.382 0.96 
Inwood —0.025 0.572 0.98 
Joco —0.025 0.271 0.94 
Riding Academy —0.03 0.591 0.96 
HQ —0.028 0.39 0.88 
Plum Beach —0.024 0.338 0.93 


B. Regression statistics: log(dry weight, g) vs. log(length, mm) 


Site b a re 
Black Bank 2.837 —5.342 0.99 
Drucker S77 —5.947 0.97 
Joco 22 Dil, —4.805 0.97 
HQ 2.43 —4.416 0.95 
Plum Beach 2.893 —5.189 0.98 
Fresh Creek 2.742 —5.168 0.99 


(Riding Academy, Fresh Creek, North Channel, and Black 
Bank) show a pulse of 3-year mussels, suggesting that all 
received relatively large numbers of recruits in the 1989 
season. Since these sites are fairly distant from the entrance 
to the bay (Rockaway Inlet), which is the only external 
source of larvae, these recruits probably originated within 
Jamaica Bay. At Plum Beach (outside of Jamaica Bay) 
and at the Little Egg and HQ sites, more age classes are 
represented with less year-to-year fluctuation in numbers 
over time than at other sites within Jamaica Bay. These 
sites, located nearer the inlet, are more likely to receive 
larvae brought into the bay with tidal currents and may 
be less dependent on localized recruitment than sites in 
the central and eastern bay. 


Table 2 
Mussel density and biomass at eight sites. 


Density (m~’) 


No. 

quad- Biomass 

Site Mean SE rats CVf ID#£ (g/m’) 
North Channel MQ — t59 Ie VaS 46 D267 
Little Egg 622 72 18 494 151 308.4 
Black Bank 1888 173 NG 36r5" 225257 3795 
Drucker 1955 138 18 30 176 8214.7 
HQ 1545 85 See 2184: Wl “418.7 
Plum Beach W35. Naa 8 42.8 135 463.1 


Outer Little Egg 1215 Je its} Sb A Sa 3) 


Fresh Creek 802 109 18 57.8 268 218.2 


Tt CV = Coefficient of variation = (SD/mean) x 100. 
+ Index of dispersion = variance/mean. 


DRY BODY WEIGHT (G) 


Page 225 


—f}— FRESH CREEK 


----[]---- BLANK BANK 
——6—  Joco 
----@---- DRUCKER 


—*A— PLUM BEACH 


----f\---- HQ 


0 20 40 60 80 100 


SHELL LENGTH (MM) 
Figure 5 


Fitted curves showing the relation between dry body weight (g) 
and shell length (mm) for six sites in July 1991. Note that body 
weights tend to be lower in populations from central Jamaica 
Bay. Curves are produced using linear regression coefficients for 
the equation: log(DW) = a + b(log length). 


Population density (Table 2) was variable and all pop- 
ulations were highly clumped. Coefficients of variability 
(CV = SD/mean x 100) ranged from 21 to 73% and 
coefficients of dispersion (CD = s*/mean) ranged from 71 
to 496. Densities were statistically different among Ja- 
maica Bay sites (Kruskall-Wallis statistic = 48.91, P = 
<0.001) and fell within the range of maximum Geukensia 
densities reported by others working in the New England 
to northern Middle-Atlantic region (FELL et al., 1982; 
BERTNESS, 1984; BERTNESS & GROSHOLZ, 1985). Com- 
paring density data between studies is problematic; how- 
ever, the Jamaica Bay marsh flat densities seem much 
greater than those in the eastern Long Island Sound marsh- 
es investigated by FELL et al. (1982) but similar to the 
western Long Island Sound marshes (and to the Narra- 
gansett Bay site studied by BERTNESS, 1984). 

Estimates of biomass for Jamaica Bay mussel popula- 
tions were lower than those reported by FELL et al. (1982) 
for the the Great Meadows and Branford marshes in west- 


Page 226 


100 


90 


80 


70 


60 


50 


Rl 


40 
CT 


MEAN SHELL LENGTH (MM) 


30 JB(HQ) 


JB(PLUM BEACH) 


20 
JB(NORTH CHANNEL) 


10 


Oa 213 4°85) 1657 89 10) Ail 12 


The Veliger, Vol. 36, No. 3 


TOMS COVE 
CAPE CHARLES 
CRISFIELD 
JB(PLUM BEACH) 


JB(DRUCKER) 


23 4 5 6 7 8 9 10 11 1243 


MUSSEL AGE (YEARS) 


Figure 6 


A. Cumulative growth curves for two within-bay sites (HQ, 
North Channel) and a site from the Rockaway Inlet outside 
Jamaica Bay (Plum Beach) compared with literature data for 
Rhode Island (BERTNESS & GROSHOLZ, 1985) and Connecticut 
(BROUSSEAU, 1984). Note that within-bay sites show lower growth 
rates. 


ern Long Island Sound. There was no statistically signif- 
icant correlation between mussel density and biomass in 
Jamaica Bay, whereas these appear to be positively cor- 
related in the Connecticut marshes studied by FELL et al. 
(1982). This suggests that environmental factors in ad- 
dition to crowding determine mussel biomass in Jamaica 
Bay. 

There are few appropriate data on the growth rates of 
Geukensia demissa that can be compared with Jamaica Bay. 
In Figure 6, growth curves of Jamaica Bay mussels are 
superimposed on published growth curves for mussels from 
Connecticut (BROUSSEAU, 1984), Rhode Island (BERTNESS 
& GROSHOLZ, 1985), and the Chesapeake Bay area 
(BERTNESS, 1980). The New England mussel populations 
(Connecticut, Rhode Island) have higher growth rates than 
all inter- Jamaica Bay populations, but are similar to Plum 
Beach (Figure 6a). However, all of the Chesapeake Bay 
area populations exceed Jamaica Bay growth rates, in- 
cluding the Crisfield site, located well within Chesapeake 
Bay. BERTNESS (1980) suggested that differences in growth 
rates in his study reflected habitat-related physical differ- 
ences among sites, including food quantity and quality. 

Our results indicate that the mussels at Plum Beach 
(outside of Jamaica Bay) grew at rates comparable to those 


B. Similar data comparing Jamaica Bay and Rockaway Inlet 
sites with published growth curves for three sites inside and 
outside of Chesapeake Bay (curves redrawn from BERTNESS, 
1980). Note that the within-bay site (represented here by Druck- 
er) is lower than all Chesapeake sites, but that growth at Plum 
Beach (outside of Jamaica Bay) is similar to the Crisfield site 
(within Chesapeake Bay). 


in other northeastern American populations. However, 
mussels within Jamaica Bay grew more slowly, and size- 
specific body weights of mussels in central bay populations 
were depressed relative to mussels in populations in the 
Rockaway Inlet (Plum Beach). 

We propose and briefly discuss four hypotheses which, 
either singly or in combination, may account for depressed 
growth rates within Jamaica Bay: (1) Mussels in the cen- 
tral core of Jamaica Bay may be more crowded than in 
populations outside of the bay; (2) The vertical shore level 
of the marsh flat at sites within Jamaica Bay may be higher 
than at sites outside of Jamaica Bay; (3) Mussel popu- 
lations within Jamaica Bay may utilize a qualitatively 
and/or quantitatively different phytoplankton population 
from mussels populations outside of Jamaica Bay; (4) 
Mussel populations in Jamaica Bay may be stressed as a 
result of long-term exposure to toxic heavy metals, poly- 
aromatic hydrocarbons, or other chemical pollutants. 

By experimentally manipulating mussels in the size range 
of 30 to 100 mm, BERTNESS & GROSHOLZ (1985) were 
able to show that mussels at high experimental densities 
(1600 m~*) grew more slowly than mussels at low density 
(400 m~*). However, the crowding effect on growth was 
smaller than the effect of shore level—z.e., in spite of greater 


PD Rerranz ej, i; Manacredi, 11993 


Page 227 


crowding, mussels at the marsh edge, which could filter 
for longer periods on each tidal cycle, grew faster than 
marsh flat mussels in the low density treatment. These 
results indicate that crowding will negatively affect growth, 
but that the crowding effect may be relatively small com- 
pared to the effect of shore level. As noted above, Jamaica 
Bay sites support relatively dense populations. Moreover, 
there is a statistically significant inverse correlation be- 
tween mussel length at year-7 and mean density (7 = 
—0.71, P = <0.05). These results are consistent with the 
hypothesis of density-dependent depression of growth rates 
in Jamaica Bay. However, neither the sampling methods 
used in this study nor the numbers of samples collected 
were appropriate to test adequately this hypothesis. 

During this study, we observed that the vertical level of 
the marsh edge varies significantly among sites owing to 
differences in erosion and sediment deposition. On the basis 
of work by BERTNESS & GROSHOLZ (1985), noted above, 
as well as other unpublished data from Jamaica Bay, we 
suggest that this factor could account for some of the vari- 
ability in mussel growth rates among sites, although this 
might not explain the general depression of growth rates 
within the central bay. 

Available evidence on the species composition and pro- 
ductivity of phytoplankton in Jamaica Bay (PETERSON & 
Dam, 1986) is consistent with similar investigations in the 
Lower New York Harbor and New York Bight (MALONE, 
1977), and indicates that plankton populations shift from 
diatom-dominated assemblages in early spring to nanno- 
plankton (especially phytoflagellate)-dominated assem- 
blages in summer. Other studies (PETERSON et al., 1985) 
indicate that Geukensia populations located deeper within 
marsh-dominated estuaries may utilize greater amounts of 
detrital material than populations associated with the ma- 
jor marsh creeks and inlets, which consume larger amounts 
of phytoplankton. Accumulating evidence (e.g., STIVEN & 
KUENZLER, 1979; FRECHETTE & BOURGET, 1985) sup- 
ports a conclusion that some mussel populations may be 
food limited. Although there is no evidence at present that 
site differences in potential food quality in Jamaica Bay 
account for differences either in growth or individual body 
weight, this topic requires further study. Spatial variability 
in current velocities also may relate to food abundance and 
quality. However, tidal current velocities are high in Ja- 
maica Bay, and at present we have no evidence suggesting 
a correlation between flow rates and mussel growth. 

Jamaica Bay receives relatively large loadings of nutri- 
ents, heavy metals, PAHs, and other chemicals from many 
point and non-point sources, including two sewage treat- 
ment plants, large volumes of combined sewer overflows, 
run-off from Kennedy International Airport, and chemical 
leachates from three inactive municipal landfills (FRANZ 
& Harris, 1988). Mussels (Mytilus edulis) sampled from 
Jamaica Bay in the Mussel Watch Program (NOAA, 1989) 


exhibited high tissue concentrations of several toxic metals, 
PAHs and PCBs, some of which may induce sublethal 
stress in mussels. The possibility that depressed growth of 
Geukensia may be caused by chemical pollutants needs 
further investigation. 


ACKNOWLEDGMENTS 


We gratefully thank student assistants Philip Ficara and 
Karina Nielsen. This research was supported in part by 
contract PX1770-1-0376 from the Gateway National Rec- 
reation Area, U.S. National Park Service. 


LITERATURE CITED 


BERTNESS, M. D. 1980. Growth and mortality in the ribbed 
mussel Geukensia demissa (Bivalvia: Dreissenacea). The Ve- 
liger 23:62-69. 

BERTNESS, M. D. 1984. Ribbed mussels and Spartina alterni- 
flora production in a New England salt marsh. Ecology 65: 
1794-1807. 

BERTNESS, M. D. & E. GROSHOLZ. 1985. Population dynamics 
of the ribbed mussel, Geukensia demissa: the costs and benefits 
of an aggregated distribution. Oecologia 67:192-204. 

BroussEAuU, D. J. 1984. Age and growth rate determinations 
for the Atlantic ribbed mussel, Geukensia demissa Dillwyn 
(Bivalvia: Mytilidae). Estuaries 7:233-241. 

FELL, P. E., N. GC. OLMSTEAD, E. CARLSON, W. Jacos, D. 
Hitcucock & G. SILBER. 1982. Distribution and abun- 
dance of macroinvertebrates on certain Connecticut tidal 
marshes, with emphasis on dominant mollusks. Estuaries 
5:234-239. 

FRANZ, D. R. & W. H. Harris. 1988. Seasonal and spatial 
variability in macrobenthos communities in Jamaica Bay, 
New York—an urban estuary. Estuaries 11:15-28. 

FRECHETTE, M. & E. BOURGET. 1985. Food-limited growth 
of Mytilus edulis L. in relation to the benthic boundary layer. 
Canadian Journal of Fisheries and Aquatic Science 42:1166- 
1170. 

Lutz, R. & M. CasTaGna. 1980. Age composition and growth 
rate of a mussel (Geukensia demissa) population in a Virginia 
salt marsh. Journal of Mollucan Studies 46:106-115. 

MALonE, T.C. 1977. Environmental regulation of phytoplank- 
ton productivity in the Lower Hudson Estuary. Estuarine 
and Coastal Marine Science 5:157-171. 

NOAA. 1989. A Summary of data on tissue contamination 
from the first three years (1986-1988) of the mussel watch 
project. National Status & Trends Program, NOAA Tech- 
nical Memorandum NOS ONA 49. 400 pp. 

PETERSON, B. J.. R. W. HowarRTH & R. H. GarritT. 1985. 
Multiple stable isotopes used to trace the flow of organic 
matter in estuarine food chains. Science 277:1361-1363. 

PETERSON, W. T. & H. G. DAM. 1986. Hydrography and 
plankton of Jamaica Bay, New York. Gateway Institute for 
Natural Resource Sciences, GATE-N-021-III, U.S. Na- 
tional Park Service. 21 pp. 

STIVEN, A. E. & E. J. KUENZLER. 1979. The response of two 
salt marsh mollusks, Littorina irrorata and Geukensia demissa, 
to field manipulations of density and Spartina litter. Ecolog- 
ical Monographs 49:151-171. 


The Veliger 36(3):228-235 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Maturation Processes in Female 


Loligo bleekert Keferstein 
(Mollusca: Cephalopoda) 


GYEONG HUN BAEG, YASUNORI SAKURAI, AND KENJI SHIMAZAKI 


Research Institute of North Pacific Fisheries, Faculty of Fisheries, 
Hokkaido University, Hakkodate, Hokkaido, 041 Japan 


Abstract. Maturing oocytes of the squid Loligo bleekert were cytologically described depending on 
the degree of formation and development of oocytes and associated follicle cells. Sexual maturity was 
defined with histological observations and divided into five phases: Phase I-V. The composition of oocytes 
in ovaries revealed that oocyte development was highly asynchronous. Seasonal changes of the five phases 
of maturity revealed that the final maturation of L. bleekeri was completed in a short period of its life 


history. 


INTRODUCTION 


The maturation process in squid has been studied in var- 
ious species, including Loligo peale: (SELMAN & ARNOLD, 
1977), L. opalescens (KNIPE & BEEMAN, 1978), L. vulgaris 
(SAUER & LIPINSKI, 1990), Lolliguncula brevis (COWDEN, 
1968), and Todarodes pacificus (TAKAHASHI & YAHATA, 
1973; IKEDA et al., 1991). In particular, SELMAN & ARNOLD 
(1977), using both light and electron microscopical tech- 
niques, defined distinct maturation stages according to the 
structure of the follicle. 

Loligo bleekeri is endemic to the western North Pacific 
and is one of the few loliginid squids adapted to cool water 
(NATSUKARI & TASHIRO, 1991). A number of ecological 
and biological aspects of the species have been investigated 
by various researchers (for review of the literature see 
NATSUKARI & ‘TASHIRO, 1991): distribution, migration, 
growth and life span based on the statolith analysis, mat- 
uration, and reproduction (including mating and spawning 
behavior, spawning season, and spawning ground). A Go- 
nado-somatic Index or the color and thickness of the re- 
productive organs were recommended as the best indices 
of sexual maturity in L. bleekeri: because they are easily 
determined, even though no histological evidence has been 
presented. In L. bleekeri, there is no information on the 
maturation process based upon histological observation. 

The purpose of our study is to describe the maturation 


process in Loligo bleekeri, based upon cytological and his- 
tological observation. 


MATERIALS anpD METHODS 


Specimens of Loligo bleekeri in northern Japan were col- 
lected by set nets or bottom trawls from the coastal waters 
of southern Hokkaido: Usujiri; Fukushima; Matsumae 
(local spawning ground), and the coast of Azigasawa, dur- 
ing 1990 and 1991 (Figure 1). For this study, a total of 
108 females ranging from 68 to 282 mm in dorsal mantle 
length (ML) were used. Reproductive organs and total 
body were weighed in order to calculate the Total Gonado- 
somatic Index: TGSI = [(ovary wt + oviduct (+ gland) 
wt)/body wt] x 100. Length was measured as ML. Ova- 
ries (108), fixed in Bouin’s solution, were sliced at 6-7 um 
in thickness. For observation, sections were stained with 
Delafield’s hematoxylin and eosin. The Periodic Acid- 
Schiff (PAS) technique was utilized to stain for polysac- 
charides. 

In Loligo bleekert, the appropriate maturity index is 
TGSI rather than GSI, because when a female becomes 
sexually mature, ripe eggs are released from the ovary and 
are stored in the oviduct until egg-laying occurs. Serial 
tissue slices for each specimen were obtained, a well-formed 
slice was selected, maturity was determined, and the com- 
position of germ cells at each phase of sexual maturity was 


Gar Baes et al 11993 


Page 229 


calculated by counting the germ cells (those having their 
nuclei and being in good condition) at various stages. 


RESULTS 
General Anatomy of the Ovary 


The ovary of Loligo bleeker: lies in the coelomic space 
at the apex of the mantle and is suspended by connective 
tissue mid-laterally and dorso-posteriorly. The ovarian 
structure consists of a main axis of central connective tissue 
with a large number of branches. Germ cells are clustered 
around the branches of connective tissue like bunches of 
grapes. 


Cytological Description of Maturing Oocytes 


Oocytes were conveniently distinguished into eight stages 
(stage 1-8) based upon the degree of formation and de- 
velopment of the oocytes and associated follicle cells. Oo- 
cytes at various stages were described below. 


Stage 1. Oogonium production (Figure 2A): Secondary oo- 
gonia (ca. 35 wm in the long axis) have a well-defined 
germinal vesicle (ca. 27 wm) surrounded by a thin layer 
of pale-staining cytoplasm. The large nucleus contains 
scattered chromatin materials. 


Stage 2. Primary growth (Figure 2B, C): The youngest 
oocytes are ca. 50-80 um in diameter. The centrally located 
nuclei (ca. 40-45 um) usually possess several prominent 
spherical and irregularly shaped nucleoli (ca. 5-7 um). 
One or two squamous follicle cells are attached to the 
surface of the growing oocyte. The follicle cells are ca. 12 
um and the oocytes ca. 140-220 um in diameter. Attach- 
ment and multiplication of a follicular cap appeared to 
develop first at the vegetative pole of the oocyte. A large 
nucleus (ca. 70-100 wm) is surrounded by an irregular 
corona. 


Stage 3. Follicle cell multiplication (Figure 2D): A contig- 
uous layer of follicle cells has completely surrounded the 
oocyte (ca. 220-330 um). The follicle cells continue to 
increase in number, and change from squamous to colum- 
nar in shape. Red stained blood vessels are observed on 
the follicular epithelium. Each developing oocyte is sur- 
rounded by supportive connective tissue. 


Stage 4. Early yolkless (Figure 2E): The definitive follic- 
ular epithelium begins to penetrate the oocyte. The nucleus 
moves toward the future animal pole of the slightly ellip- 
tical-shaped oocyte. Folds of follicle cells, which enclose 
connective tissue and blood vessels, progressively invade 
the growing oocyte, with a high mitotic rate. 


Stage 5. Late yolkless (Figure 2F, G): The follicle cells, 
which show cytoplasmic basophilia, continue to elongate. 
Large multiple nucleoli appear irregularly oval, with a 
length of approximately 7 um (nuclei ca. 16 um). Indi- 
vidual follicle cells are no longer distinguished. A follicular 


JAPAN SEA 


Honshu 
Island 


Figure 1 


Sampling locations for specimens of Loligo bleekeri caught by set 
nets or bottom trawls. Azigasawa (September 1991); Usujiri (Oc- 
tober-November 1990, 1991); Fukushima (December 1990, 1991); 
Matsumae (December-February 1990, 1991). 


syncytium, which reaches a maximum height of ca. 55 wm, 
is formed. 


Stage 6. Early vitellogenesis (Figure 2H): The follicular 
syncytium is engaged in vitellogenesis and the formation 
of a chorion. Red-stained yolk bodies are distributed ran- 
domly in clusters in the oocyte. Yolk granules are numerous 
and generally appear as contiguous polyhedra (ca. 15-25 
pm). 


Stage 7. Late vitellogenesis (Figure 21, J): The follicular 
syncytium is displaced toward the periphery of the oocyte 
by the formation of the PAS-positive yolk mass. Chorionic 
particles accumulate in the interface between the follicular 
epithelium and the oocyte as discrete droplets and exhibit 
a vivid PAS reaction. By the end of this stage, oocytes are 
ca. 2.2 mm in length, and a thin cytoplasm encloses the 
yolk mass. Vitellogenesis terminates. 


Stage 8. Maturation and ovulation (Figure 2K, L): The 
formation of the chorion (ca. 37-40 um thick) is complete. 
The follicular syncytium has undergone a final degener- 
ation. Mature oocytes (ca. 2.6-2.7 mm in length) are ready 
to be released or have already been ovulated. 


Description of Sexual Maturity 


The maturity of Loligo bleekeri was divided into five 
phases on the basis of the stage of the most advanced oocytes 
in ovaries because oocyte development of the species is 


Page 230 The Veliger, Vol. 36, No. 3 


mate 


> SSR f : 
MART 


Photomicrographs of germ cells in female Loligo bleekeri at various stages of development. A (stage 1). Germ cell 
at the oogonium production stage, scale line 2.6 wm. B, C (stage 2). B. Young oocyte at the primary growth stage. 
Large nucleus (nu) contains several prominent spherical and irregularly shaped nucleoli(n), scale line 5.6 um. C. 
Oocyte at the late primary growth stage. Follicle cell cap (fcc) on vegetative pole, scale line 114m. D (stage 3). 
Oocytes at the follicle cell (fc)-multiplication stage, scale line 25 wm. E (stage 4). Oocyte at the early yolkless stage. 
Invagination of follicular epithelium begun, scale line 17.9 um. F, G (stage 5). F. Oocyte at the late yolkless stage. 
Micropyle lens (ml), scale line 20.9 um. G. Follicular syncytium is formed with large nuclei and irregularly oval 
nucleoli (n), scale line 20.9 wm. H (stage 6). Oocyte at the early vitellogenesis stage. Yolk granules (y), scale line 
62.5 um. I, J (stage 7). I. PAS positive oocyte at the late vitellogenesis stage. Nucleus (nu) of follicular syncytium, 


Figure 2 


GyH= Baes er aly 1993 


Table 1 


Maturational changes during the eight stages of oocyte development in female Loligo bleekert. 


Matu- 
ML TGSI rity 
Date (mm) (%) phase 1 2 

11 Sep 91 68 0.18 I + 100.00 
11 Sep 91 76 0.17 I ap 100.00 
11 Sep 91 103 0.16 I + 100.00 
10 Oct 90 133 0.27 II + 37.97 
29 Oct 91 183 0.47 II + 42.53 
21 Nov 90 174 0.39 II + 35.87 
29 Oct 91 173 0.19 Ill 3.61 
21 Nov 90 163 0.78 III 2.20 
14 Dec 91 184 1.08 Ill 
14 Dec 91 182 1.65 IV 
14 Dec 91 177 1.84 IV 
06 Dec 90 223 4.28 IV 
06 Dec 90 244 8.25 Vv 
06 Dec 90 223 12.67 Vv 
20 Dec 90 241 8.75 Vv 
30 Jan 91 264 8.49 Vv 
20 Dec 90 259 10.43 Vv 
30 Jan 91 263 9.56 V 
20 Feb 91 214 9.25 Vv 
20 Feb 91 209 25 V 


ML: Dorsal mantle length; TGSI: Total gonado-somatic index. 


asynchronous. The oocytes used as phasing criteria fol- 
lowed those of SELMAN & ARNOLD (1977). Table 1 reveals 
the stage composition of oocytes in ovaries of maturing 
females. All oocytes at the primary growth stage (stage 2) 
gradually transferred to ones at the more advanced stages 
during maturation, and, consequently, oocytes in the ear- 
lier stages as well as oogonia were not found in the ovaries 
of fully mature females. 


Phase I (Figure 3A, Table 1): The most advanced oocytes 
are at the primary growth stage (stage 2). A few germ 
cells at the oogonium production stage (stage 1) are found. 


Phase II (Figure 3B, Table 1): The most advanced oocytes 
are at the follicle cell-multiplication stage (stage 3). The 
number of oogonia and oocytes at the primary growth stage 
(stage 2) have decreased prominently. Most oocytes are in 
the follicle cell-multiplication stage. 


Phase III (Figure 3C, Table 1): The most advanced oo- 
cytes are at the late yolkless stage (stage 5). The number 
of oocytes at the follicle cell-multiplication stage (stage 3) 
has diminished with maturation. Oocytes in the primary 
growth stage (stage 2) still exist in low numbers. Recruit- 
ment to the primary growth stage is completed and oogonia 
are no longer observed. 


Page 231 
Stage of oocyte development (%) Gunle: 

4 5 6 7 8 tion 

62.03 = 
57.47 — 
64.13 = 
66.27 24.10 6.01 — 
36.26 39.56 21.98 = 
38.78 30.61 30.61 = 
2.56 61.54 17.94 10.26 7.70 = 
6.67 45.00 35.00 6.67 6.66 = 
48.72 33.33 7.70 10.25 = 

15.00 35.00 10.00 40.00 + 

1.43 3.33 42.86 52.38 + 

3.45 7.66 22.22 66.67 + 

16.00 32.00 12.00 40.00 + 

Seip 7.62 6.67 66.67 13.33 te 

298) 7.70 12.22 72.22 5.56 ar 

6.67 6.67 6.67 5223, 4.76 + 

17.39 30.43 8.70 36.07 7.41 “F 


Phase IV (Figure 3D, Table 1): Oocytes in various stages 
coexist in different proportions in the ovary. Oocytes in 
the late vitellogenesis stage (stage 7) are the most devel- 
oped. Oocytes at the primary growth stage (stage 2) and 
follicle cell-multiplication stage (stage 3) are rarely or 
never found. Most oocytes at the follicle cell-multiplication 
stage have developed to the yolkless stage. 


Phase V (Figure 3E, Table 1): Oocytes in various stages 
from the follicle cell-multiplication stage (stage 3) to the 
maturation and ovulation stage (stage 8) coexist in the 
ovary; however, oocytes at the follicle cell-multiplication 
stage are never found and oocytes at the early yolkless 
stage (stage 4) are observed in relatively low numbers. 
Recruitment to the follicle cell-multiplication stage does 
not occur, owing to the absence of oocytes at the primary 
growth stage (stage 2). 


Seasonal Changes of the Maturity Composition 


Figure 4 indicates the phase of maturity of Loligo bleekeri 
specimens collected periodically. Females at phase I were 
identified in September. The females had a mean ML of 
92 mm and showed a very low TGSI (Table 2). The modal 
size of females at phase II was between 99 and 177 mm, 


scale line 83 wm. J. Chorionic particles (cp) at the interface region, scale line 20.9 um. K, L (stage 8). K. Degenerating 
follicular syncytium (df) and completed chorion (c), scale line 20.9 wm. L. Ripe oocyte, scale line 125 um. 


Page 232 


The Veliger, Vol. 36, No. 3 


Figure 3 


Photomicrographs of cross sections through ovaries in the various stages of maturity. A (phase I). Scale line 41.7 
um. B (phase II). pr, oocyte at the primary growth stage (stage 2); fm, oocyte at the follicle cell-multiplication stage 
(stage 3), scale line 41.7 um. C (phase III). ey, oocyte at the early yolkless stage (stage 4), ly, oocyte at the late 
yolkless stage (stage 5), scale line 41.7 wm. D (phase IV). ev, oocyte at the early vitellogenesis stage (stage 6), lv, 
oocyte at the late vitellogenesis stage (stage 7), scale line 238 um. E (phase V). m, oocyte at the maturation and 


ovulation stage (stage 8), scale line 277.8 um. 


and the TGSI composition of the females showed a slight 
increase. This phase of maturity appeared in middle Sep- 
tember and extended to late November. Phase III appeared 
first in late October and predominated through November. 
Phase III females showed a wide range of variation in 
length composition and a continuous increase in TGSI 
value. Phase IV was found from late November to middle 
December. This is an indication that active vitellogenesis 
is completed in a very short period. Phase IV females 
showed a significant increase in their TGSI value com- 
pared with that of the previous phase and ranged in ML 
from 177 to 233 mm. Squids at phase V were the major 
components of the population on the spawning ground. 
Phase V females were found from December to February, 
revealed a high TGSI with extreme fluctuations, and 
showed a significant increase in ML composition. 

TSGI and ML values of females at the various phases 
of maturity were plotted in Figure 5. Although modal size 
at each phase overlapped, TGSI composition was clearly 


separated between females at phases I-III and at phases 
IV-V. Female Loligo bleeker: at phases IV-V are defined 
by TGSI values greater than 1.5% and ML greater than 
175 mm. Phase V females of L. bleekeri are easily distin- 
guished by the presence of ripe eggs in the oviduct. 


DISCUSSION 


The pattern of oocyte development observed in Loligo 
bleekert is nearly identical to those of Lolliguncula brevis 
(COWDEN, 1968), Loligo pealei (SELMAN & ARNOLD, 1977), 
Loligo opalescens (KNIPE & BEEMAN, 1978), and Loligo 
vulgaris (SAUER & LIPINSKI, 1990). Oogenesis in cepha- 
lopod mollusks involves a highly coordinated differentia- 
tion of the oocyte and follicular epithelium (SELMAN & 
ARNOLD, 1977). Several morphological and histological 
studies have elucidated the functions of follicle cells in 
mollusks: vitellogenesis (O’DoR & WELLS, 1973, 1975; 
SELMAN & WALLACE, 1978); the formation of the second- 


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MATURITY 

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Page 233 


Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. 


MONTH 


Figure 4 


Seasonal changes of the five phases of maturity in female Loligo bleekeri. 


ary egg membrane (SELWOOD, 1968, 1970; BOTTKE, 1974; 
SELMAN & ARNOLD, 1977); the ovulation process (DE 
JONG-BRINK et al., 1976); phagocytosis (SELWOOD, 1968, 
1970); hormone production (RUNHAM et al., 1973); the 
origins of the animal-vegetal and bilateral symmetries of 
the egg (RAVEN, 1966); and transportation of the oocyte 
(DE JONG-BRINK et al., 1976). 

Chronological differences in vitellogenesis exist between 
Loligo bleekert and Todarodes pacificus. In L. bleekeri, as in 
many other loliginid species, follicle cells occupy most of 
the volume of the entire oocyte-follicle complex; subse- 
quently, individual follicle cells fuse to form a syncytium, 
which is engaged in vitellogenesis (Figure 2G). On the 
other hand, the follicular syncytium in females of 7. pa- 
cificus is formed when follicle cells occupy a relatively small 
volume of the oocyte-follicle complex and participate in 
vitellogenesis (TAKAHASHI & YAHATA, 1973; IKEDA et al., 
1991). The oocyte-follicle complex of 7. pacificus approx- 
imately corresponds to the one at the early yolkless stage 
(stage 4, Figure 2E) in L. bleekert. In particular, TAKA- 
HASHI & YAHATA (1973) revealed the existence of a yolk 
nucleus in oocytes corresponding to ones at the primary 
growth stage (stage 2, Figure 2C) in L. bleeker:. The above- 
mentioned chronological differences seem to be due to 
prominent difference in the size of oocytes between the 
two species. Fundamentally, the oocyte development of L. 
bleekert is identical to that of 7. pacificus, except for the 
vitellogenic process. 


The existence of polysaccharid material in the yolk gran- 
ules of Loligo bleekeri is indicated by the vivid PAS reaction 
seen in Figure 3D. Cytochemical investigations on the 
composition of yolk in mollusks (z.e., FUjm, 1960; RAVEN, 
1961; COWDEN, 1961, 1962, 1968; DONATO CELI, 1967; 
UBBELS, 1968) have established that yolk granules contain 
carbohydrates, muco- or glycoproteins, iron-containing 
proteins, phospholipids, and particular amino acids (ty- 
rosine, tryptophan, arginine). 

An analysis of the reproductive cycle of Loligo bleekeri 


Table 2 


The range of TGSI and ML of female Loligo bleekeri at 
the various phases of maturity. 


Maturity TGSI (%) ML (mm) 

phase (range + SD) (range + SD) 

I 0.13 92 
(0.02-0.24 + 0.08) (68-105 + 12) 

Il 0.37 1133 
(0.1-0.71 + 0.19) O9=1ii + 22) 

Ill 0.7 168 
(0.19-1.28 + 0.27) (132-222 + 19) 

IV 2.48 195 
(1.58-4.28 + 0.81) (177-223 + 16) 

Vv 9.96 249 


(5.16-16.45 + 3.12) (209-282 + 20) 


TGSI: Total gonado-somatic index; ML: Dorsal mantle length. 


Page 234 


The Veliger, Vol. 36, No. 3 


150 177 200 250 300 
ML(mm) 


Figure 5 


Relation between TGSI and ML of female Loligo bleekeri at the various phases of maturity. TGSI: Total Gonado- 


somatic Index; ML: Dorsal Mantle Length. 


demonstrated that active vitellogenesis was completed in a 
single month. This is an indication of high meiotic rate of 
oocytes at the vitellogenesis stage. Ovaries of fully mature 
females are occupied (ca. 75%) mostly by oocytes at the 
vitellogenesis stage. From the above facts, it may be con- 
sidered that the oocytes function as recruitment to ripe 
eggs, which are used in the series of egg-layings. However, 
it has not been determined whether L. bleekeri spawns in 
series during only one spawning season. 

WAKUTSUBO (1989) reported that two different spawn- 
ing populations coexist on the northern coast of Honshu 
(Aomori Prefecture). One cohort spawns in winter (winter 
population, range from December to February) and the 
other cohort spawns in spring (spring population, range 
from March to June). Animals used in this study probably 
belong to the winter-spawning population, based on clear 
seasonal changes in maturity, ML, and TGSI values. The 
range of TGSI values of phase V females is extremely 
wide (5.16-16.45%). This may indicate that egg devel- 
opment is highly asynchronous among individuals and that 
females of Loligo bleekeri are in fact serial spawners. Based 
on seasonal changes in maturity and ML composition, the 
life span of L. bleekeri is thought to be one year. 


ACKNOWLEDGMENTS 


We gratefully acknowledge Dr. H. Munehara, Usujiri 
Fisheries laboratory, Hokkaido University, for critical 
reading of the manuscript and some suggestions. 


LITERATURE CITED 


BoTTKE, W. 1974. The fine structure of the ovarian follicle of 
Alloteuthis subulata Lam. (Mollusca, Cephalopoda). Cell and 
Tissue Research 150:463-479. 

CowDeEN, R.D. 1961. A cytochemical investigation of oogenesis 
and development to swimming larval stage of the chiton in 
Chiton tuberculatum. Biological Bulletin 120:313-325. 

CowDEN, R. D. 1962. Further cytochemical investigations on 
the growth and development of slug oocytes. Growth 26: 
209-234. 

CowDEN, R. D. 1968. Cytological and cytochemical studies of 
oocyte development and development of the follicular epi- 
thelium in the squid, Loligo brevis. Acta Embryologiae et 
Morphologiae Experimentalis 10:160-173. 

DONATO CELI, A. 1967. Ulteriore contributo alla conoscenza 
della natura chimica dei globule vitellini di Aplysia depilans 
L. (Moll. Gast. Opis.). Acta Histochemica 26:205-209. 

FieLps, W. G. 1965. The structure, development, food rela- 
tions, reproduction, and life history of the squid Loligo opa- 
lescens Berry. California Department Fish & Game, Fishery 
Bulletin 131:1-108. 

Fuji, T. 1960. Comparative biochemical studies on the egg- 
yolk proteins of various animal species. Acta Embryologiae 
et Morphologiae Experimentalis 3:260-285. 

IKEDA, Y., Y. SAKURAI & K. SHIMAZAKI. 1991. Development 
of female reproductive organs during sexual maturation in 
the Japanese common squid Todarodes pacificus. Nippon 
Suisan Gakkaish (Bulletin of the Japanese Society of Sci- 
entific Fisheries) 57(12):2243-3347 [in Japanese with En- 
glish title and abstract]. 

JONG-BrINK, M. DE, A. WIT, G. KRAAL & H. H. BOER. 1976. 
A light and electron microscope study on oogenesis in the 


G. H. Baeg et al., 1993 


freshwater pulmonate snail Biomphalaria glabrata. Cell and 
Tissue Research 171:195-219. 

KnIPE, J. H. & R. D. BEEMAN. 1978. Histological observations 
on oogenesis in Loligo opalescens. California Department Fish 
& Game, Fishery Bulletin 169:23-33. 

NaTsuKaRI, T. & M. TAsHIRO. 1991. Neritic squid resources 
and cuttlefish resources in Japan. Marine Behavior and 
Physiology 18:149-226. 

O’Dor, R. K. & M. J. WELLS. 1973. Yolk protein synthesis 
in the ovary of Octopus vulgaris and its control by the optic 
gland gonadotropin. Journal of Experimental Biology 59: 
665-674. 

O’Dor, R. K. & M. J. WELLS. 1975. Control of yolk protein 
synthesis by Octopus gonadotropin in vivo and in vitro (effects 
of Octopus gonadotropin). General and Comparative En- 
docrinology 27:129-153. 

RAVEN, C. P. 1961. Oogenesis. The Storage of Developmental 
Information. Pergamon: Oxford, London, New York, and 
Paris. 

RAVEN, C. P. 1966. Morphogenesis. The analysis of Molluscan 
development. 2nd ed. Macmillan (Pergamon): New York. 

RUNHAM, N. W., T. G. BAILEY & A. A. LARYEA. 1973. Studies 
on the endocrine control of the reproductive tract of the grey 
field slug Agriolimax reticulatus. Malacologia 14:135-142. 

SAUER, W.H.& M.R. Lipinski. 1990. Histological validation 
of morphological stages of sexual maturity in chokker squid 


Page 235 


Loligo vulgaris Reynaudii D’orb (Cephalopoda: Loliginidae). 
South African Journal of Marine Science 9:189-200. 
SELMAN, K. & J. M. ARNOLD. 1977. An ultrastructural and 
cytochemical analysis of oogenesis in the squid, Lolzgo pealei. 

Journal of Morphology 152:381-400. 

SELMAN, K. & R. A. WALLACE. 1978. An autoradiographic 
study of vitellogenesis in the squid Loligo pealei. Tissue and 
Cell 10:599-608. 

SELWoOoD, L. 1968. Interrelationships between developing oo- 
cytes and ovarian tissues in the chiton Sypharochiton septen- 
triones (Ashby) (Mollusca, Polyplacophora). Journal of 
Morphology 125:71-104. 

SELWoop, L. 1970. The role of the follicle cells during oogenesis 
in the chiton Sypharochiton septentriones (Ashby) (Polypla- 
cophora, Mollusca). Zeitschrift fur Zellforschung und Mik- 
roskopische Anatomie 104:178-192. 

TAKAHASHI, N. & T. YAHATA. 1973. Histological studies on 
the maturation of the ovary in the squid, 7odarodes pacificus. 
Bulletin of the Faculty of Fisheries Hokkaido University 
24(2):63-68. 

UBBELS, G. A. 1968. A cytochemical study of oogenesis in the 
pond snail Limnaea stagnalis. Thesis, Utrecht. 

WakutTsuso, T. 1989. Migration of the squids Loligo bleekert 
around the coast of Aomori Prefecture. Report of Japan Sea 
Regional Fisheries Research Laboratory:34-40. [In Japa- 
nese. | 


The Veliger 36(3):236-244 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A Comparison of Larval Development, Growth, and 


Shell Morphology in ‘Three Caribbean 
Strombus Species 
by 


MEGAN DAVIS, CYNTHIA A. BOLTON, anp ALLAN W. STONER 


Caribbean Marine Research Center, 805 E. 46th Place, Vero Beach, Florida 32963, USA 


Abstract. Development, growth rates, and shell morphology are compared for the larvae of the three 
most abundant Strombus species living in the Bahamas: S. gigas, S. costatus, and S. raninus. Illustrations 
are provided for positive identifications of the larval shells from field studies. Maximum shell dimensions 
of S. costatus, S. gigas, and S. raninus differ significantly at hatching (388 + 14 wm SL, 354 + 15 wm 
SL, and 197 + 8 wm SL, respectively). The shell length (SL) for these species at competence was 
correlated with developmental time to competence in laboratory culture (7? = 0.95). Strombus raninus 
had the largest shell at competence (1450 + 53 um SL) and the longest larval cycle (40 days). Strombus 
costatus was 14% smaller (1277 + 101 um SL) and was competent at 32 days, while S. gigas had the 
smallest shell at competence (1170 + 58 um SL) and the shortest larval period (21 days). These 
differences in developmental rate suggest species-specific differences in potential larval dispersal and 


recruitment processes. 


INTRODUCTION 


In recent years there has been increasing interest in the 
larval ecology of the queen conch, Strombus gigas Linnaeus, 
1758. This stems from a need to understand the ecology 
and recruitment dynamics of this severely overfished Ca- 
ribbean resource (BERG & OLSEN, 1989; APPELDOORN & 
RODRIGUEZ, 1992) and an interest in stock rehabilitation 
through release of hatchery-reared juveniles (BERG, 1976; 
APPELDOORN & BALLANTINE, 1983; SIDDALL, 1984; DAVIS 
et al., 1987). Eggs (ROBERTSON, 1959), spawning 
(RANDALL, 1964), and larval development (D’AsaAro, 1965) 
of S. gigas have been described for over 25 years; however, 
the first reports of distribution and abundance of S. gigas 
veligers were published during the last year (CHAPLIN & 
SANDT, 1992; STONER et al., 1992a; POSADA & APPEL- 
DOORN, 1992). 

Seven Strombus species inhabit the warm subtropical 
and tropical waters of the western north Atlantic Ocean, 
and the biogeography and taxonomic characteristics for 
adults have been compared (CLENCH & ABBOTT, 1941; 
ABBOTT, 1974; WALLS, 1980; MOSCATELLI, 1987). In the 
Bahamas, the three most abundant Strombus species are 
S. gigas (queen conch), S. costatus Gmelin, 1791 (milk 
conch), and S. raninus Gmelin, 1791 (hawk wing conch), 


all of which spawn during the summer (Stoner, personal 
observations). 

The objectives of this study were to compare the larval 
shell morphologies of Strombus gigas, S. costatus, and S. 
raninus to assist in positive identifications for field studies, 
and to compare their development and growth rates in 
laboratory culture. Differences in growth rates and time 
to competence are discussed in terms of potential larval 
dispersal and recruitment processes. 


MATERIALS anp METHODS 


To compare larval development, Strombus gigas, S. raninus, 
and §. costatus were cultured at the Caribbean Marine 
Research Center (CMRC) in Vero Beach, Florida, be- 
tween May and September 1992, using culture techniques 
adapted from Davis (1992). Culture temperature was 27- 
30°C, salinity was constant at 35%o, photoperiod was 12L: 
12D, and seawater was purified with a 10-um filter and 
ultraviolet sterilizer. 

Newly laid egg masses of Strombus gigas and S. costatus 
were collected near the CMRC field station on Lee Stock- 
ing Island, Exuma Cays, Bahamas. Strombus gigas masses 
were found on an 18-m deep, coarse-sand breeding site 
east of the island (STONER & SANDT, 1992). Strombus 


M. Davis et al., 1993 


costatus masses were found on a 2-m deep sandy shoal 
northwest of the island. Egg masses, collected either the 
day before or on the morning of shipment, were sent by 
air to Vero Beach in individual insulated bottles containing 
about 500 mL of seawater at 26°C. For S. raninus, nine 
mature females and two males were collected in the vicinity 
of Lee Stocking Island and transported to the CMRC Vero 
Beach Laboratory. This reproductive stock was main- 
tained in a flow-through downwelling sand tray and fed 
a variety of macroalgae (primarily Enteromorpha sp.). The 
sand trays were searched daily for egg masses. Portions of 
two or three egg masses were cultured for each species. 
Egg masses were incubated in flow-through upwelling 
containers. A section of egg mass strand was observed daily 
under a compound microscope (100 x ) to determine hatch 
day. Capsulated veligers were ready to hatch when they 
were observed rotating in their egg capsules; and their 
velar lobes, eye spots, and orange foot pigments were clear- 
ly visible (D’Asaro, 1965; Davis, 1992). Within 24 hr of 
an expected hatch (3-4 days after spawning) several 2-3 
cm egg strands were placed in two 1-L beakers (1000 mL 
seawater/beaker). Approximately 12 hr after emergence, 
which usually occurred in the early evening, swimming 
veligers were siphoned into a 73-um seive which was par- 
tially submerged in a seawater-filled container to ease lar- 
val stress and prevent shell damage. The veligers were 
rinsed off the seive and initially stocked in three 1-L bea- 
kers (1000 mL seawater/beaker) at a density of 100-200 
veligers/L. Culture water was static and aeration was not 
necessary; however, veligers were transferred into clean 
water and beakers daily by using a 73- or 200-yum seive 
depending on veliger size. At each water change algal 
debris and dead veligers were removed with a pipette. 
Density was gradually reduced by diluting the cultures to 
10-20 veligers/L as the veligers neared competence. The 
veligers were cultured until they were metamorphically 
competent. Competence was recognized by observing pig- 
mentation changes on the foot (orange to green) (DAVIS, 
1992) and swim-crawl behavior (larva uses foot to move 
on substrate with lobes extended) (Davis, unpublished data). 
Larvae were fed Caicos Jsochrysis cultured with Fritz® 
media in 250-mL Erlenmeyer flasks (GUILLARD, 1975). 
Feeding began at an initial density of 5000 cells/L and 
was increased to 7000 cells/L over the culture period. The 
diet of late-stage veligers was supplemented with 3000 
cells/L of Chaetoceros gracilis Schutt. 
Egg-strand and capsule diameters were measured using 
a compound microscope with a calibrated ocular microm- 
eter (Figure 1). The number of Strombus raninus eggs per 
egg mass was estimated by separately hatching two egg 
masses in 10 L of seawater. The hatched veligers were 
stirred and five 10-mL aliquots were counted. Additional 
egg-mass data were obtained from ROBERTSON (1959), 
RANDALL (1964), and DAvIs et al. (1984). 
Approximately 10 veligers were collected daily from 
each culture, examined, and then preserved in 5% buffered 
formalin (95% seawater). Collection began on day one, 


Page 237 


Figure 1 


Egg mass strand section: c, coil of the strand; ed, egg capsule 
diameter; sd, strand diameter. 


approximately 12 hr after hatching. Although development 
of Strombus larvae is a continual process, five stages of 
larval shell development were arbitrarily chosen. ‘These 
stages were easily recognized and were used for compar- 
isons and illustrations. Stage I represented the newly 
hatched larva (protoconch I). Stage II larvae were char- 
acterized by an elongated beak; for all species this occurred 
on day 5. Stage III larvae were 530-600 um in shell length; 
they continued to have an elongated beak; and specimens 
for all three species were collected on day 10. By Stage IV 
the beaks of all species had diminished to a small point; 
S. gigas and S. costatus larvae were collected on day 15 and 
S. raninus larvae on day 20. Stage V larvae were collected 
when they became competent for metamorphosis as de- 
scribed above (days 21, 32, and 40 for S. gigas, S. costatus, 
and S. raninus, respectively); at this stage the larva! shells 
had no beak and they had reached their terminal shell 
size. Maximum shell dimension (MD) was measured for 
Stage I of each species and also for Stage II of S. raninus 
(Figure 2A). Shell length (SL) was measured for all other 
stages of each species (Figure 2B). A random sample of 
20 shells from Stages I and II, and 10 shells from Stages 
III, 1V, and V were measured using a dissecting microscope 
(20-40 x) equipped with an ocular micrometer. 

The dorsal and ventral views of the preserved larval 
shells were projected onto a computer monitor using a 


Page 238 


Figure 2 


Larval shell measurements. A. Maximum shell dimension (MD). 
B. Shell length (SL). Terminology: a, apex; b, beak; bl, beak 
line; sc, siphonal canal. 


video camera attached to a dissecting microscope (40 ). 
Individual shell images were digitized using a Macintosh 
video program (MediaGrabber®) and transferred to a 
Macintosh drawing program (Canvas®) where an outline 


The Veliger, Vol. 36, No. 3 


of each shell was drawn to proportion. Shell details seen 
with the aid of dissecting (40 x ) and compound microscopes 
(100) were added to the final drawings, which were 
prepared by a biological illustrator. 


RESULTS 
Egg Masses 


The three Strombus species examined lay similar cres- 
cent-shaped egg masses, each composed of a single strand 
of eggs folded back and forth perpendicular to the long 
axis of the crescent (ROBERTSON, 1959; D’Asaro, 1965). 
The S. gigas egg mass is slightly larger than that of S. 
costatus, but both are larger than the S. raninus egg mass 
(Table 1). Egg-strand diameter shows a similar pattern, 
wherein the diameter of the egg strand is related to the 
number of egg capsules per mm of strand length, the num- 
ber of egg capsules per coil of the strand, and egg-capsule 
size (Table 1, Figure 1). 

The rate at which the eggs develop is temperature de- 
pendent (Davis & HESsSE, 1983; RODRIGUEZ-GIL et al., 
1991), and the eggs hatch between 3 and 5 days after 
spawning at 27—30°C. In this laboratory study, fecundity 
was calculated for Strombus raninus. Nine S. raninus fe- 
males laid 51 egg masses in 46 days (24 July to 7 Sep- 
tember), an average of 3.7 egg masses per month per fe- 
male. Strombus raninus females may lay twice as many egg 
masses per month compared to S. gigas females (Table 1). 


Larval Development 


The newly hatched shells of Strombus gigas, S. raninus, 
and S. costatus were significantly different in maximum 
shell dimension (ANOVA, F,,;;, = 1287, P < 0.001) (Fig- 
ure 3), and all of the means were significantly different 


Table 1 


Comparison of egg mass characteristics for three Strombus species. Means with one standard deviation 
and sample number, n, in parentheses. 


Variables S. gigas 


8-15 (9) 
785 + 44 (10) 
313,000-485,000 (10)? 


Length of egg mass (cm) 
Diameter of egg strand (um) 
No. eggs/mass 
No. egg capsules per 

mm of strand length 
No. eggs per coil 

of the strand 5-67 
Egg capsule diameter (um) 225 + 17. (20) 
Days until hatching 


14-16 (10) 


at 27-30°C 3-4 
Fecundity (No. egg masses 
per female per month) 7S 


* ROBERTSON (1959). 
® RANDALL (1964). 
© DAVIS et al. (1984). 


Species 
S. raninus S. costatus 
4-7 (4) 6-10 (2) 


321 + 20 (10) 
206,000-245,000 (2) 


761 + 18 (10) 
185,000-210,000 (2)? 


21-25 (15) 12-14 (10) 
3a 4-53 
140 + 4 (30) 262 + 6 (20) 
3 4 
3.7 NA 


M. Davis et al., 1993 


Shell Length (ym) 


re4 


Page 239 


Strombus gigas 


Strombus costatus 


Strombus raninus 


25 30 35 40 45 50 


Age (days) 


Figure 3 


Growth curves for three larval Strombus species laboratory cultured at 27-30°C. 


(Tukey’s multiple comparisons of means, P < 0.001). 
Strombus costatus hatched with the largest maximum shell 
dimension (mean = 388 wm; SD = 14; n = 20), S. gigas 
was 9% smaller (mean = 354 wm; SD = 15; n = 20), and 
S. raninus hatched at approximately half the size of S. 
costatus (mean = 197 um; SD = 8, n = 20). 

Species differences in shell size at competence were also 
significantly different (ANOVA, F..,) = 38, P < 0.001) 
(Figure 3), and all of the means were significantly different 
(Tukey’s multiple comparisons of means, P < 0.01). At 
competence Strombus raninus had the longest SL (mean = 
1450 wm; SD = 53; n = 10), S. costatus was 14% smaller 
(mean = 1277 wm; SD = 101; n = 10), and S. gigas was 
24% smaller than S. raninus (mean = 1170 wm; SD = 58; 
n = 10). 

Strombus gigas had the fastest growth rate over the entire 


larval phase (39 wm/day), and reached competence in the 
shortest time (day 21) (Figure 3). Strombus costatus had 
an overall growth rate of 28 um/day, and reached com- 
petence in 32 days (Figure 3). Strombus raninus had an 
overall growth rate of 31 um/day, and reached competence 
in 40 days (Figure 3). Shell length for these species at 
competence was correlated (r* = 0.95) with developmental 
time to competence (z.e., S. gigas larvae were competent at 
day 21 and had the smallest shell at competence; and S. 
raninus larvae were competent at day 40 and had the largest 
shell at competence). 


Shell Morphology 


Larval shell development for Strombus gigas, S. raninus, 
and S. costatus is illustrated for the five stages described 


The Veliger, Vol. 36, No. 3 


Page 240 


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Page 241 


M. Davis et al., 1993 


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Page 242 


above (Figure 4). Details of beak lines and other markings 
are best seen by viewing the shells with a dissecting mi- 
croscope (40-60 x) and top illumination. 


Stages I and II (Figure 4, drawings 1-15): The shells of 
newly hatched veligers of Strombus gigas and S. costatus 
are difficult to distinguish, owing to their similar shape 
and size. To make accurate identifications, the shell of each 
species was positioned on edge with the apex and siphonal 
canal showing (Figure 4, drawings 2 and 7). From this 
view the SL of S. costatus is slightly longer (~60 wm) than 
that of S. gigas. More importantly, the apex of S. costatus 
protrudes like a dome from the beginning of the first whorl. 
By day 5, S. costatus whorls are laid down in a tight spiral, 
compared to those of the other two species, resulting in a 
slightly elongated larval shell (Figure 4, drawing 14). Newly 
hatched and 5-day-old shells of S. raninus are approxi- 
mately 40-50% smaller than the same age larvae of S. gigas 
and S. costatus; therefore, they cannot be confused with 
those of the other two species (Figure 3). 

Shell color also distinguishes these three species. At 
hatching Strombus gigas has a creamy, off-white, trans- 
lucent shell with small pustulate markings, S$. ranznus has 
a transparent shell with no color, and S. costatus has a 
semi-transparent shell, also with no color. All three species 
have long beaks; however, the beak lines differ (Figure 2). 
At hatching S. gigas has the most prominent beak line, 
comprised of four raised parallel lines (striae) which follow 
the beak whorl (Figure 4, drawing 2). The beak line for 
S. raninus is faint, but resembles a shaded band (Figure 
4, drawing 12). Strombus costatus also has a faint beak line 
at hatching, but it becomes more apparent by day 5. This 
beak line is similar to that of S. gigas; however, a repeated 
C-shaped pattern on the ridge, resembling growth lines, 
is a more obvious feature (Figure 4, drawings 14 and 15). 

At hatching the shells of Strombus gigas and S. costatus 
have 1.5 whorls and S. raninus has approximately 1.25 
whorls. By day 5, S. gigas has 2 whorls, S. raninus has 1.5 
whorls, and S. costatus has 2.5 whorls. 


Stage III (Figure 4, drawings 16-21): By day 10 the three 
species are similar in shell length (Figure 3), and the beaks 
are still elongated; however, the number of whorls differs. 
Strombus gigas has 2.5 whorls, S. raninus has 3.5 whorls, 
and S. costatus has 3 whorls. The beak lines on all species 
are apparent—S. gigas with parallel lines (Figure 4, draw- 
ings 16 and 17), S. raninus with a shaded band which 
protrudes slightly from the outer whorl (Figure 4, drawing 
19), and S. costatus with the repeated C-shaped pattern 
(Figure 4, drawings 20 and 21). The apex of the shell is 
an important feature for separating the species; in S. gigas 
it is round and blunt (Figure 4, drawing 16), in S. raninus 
small and pointed (Figure 4, drawing 18), and in S. costatus 
dome-shaped and tilted (Figure 4, drawing 20). The shell 
color of both S. gigas and S. costatus is now a faint amber. 
Pustulate markings persist on the S. gigas shell through 
all stages. 


The Veliger, Vol. 36, No. 3 


Stage IV (Figure 4, drawings 22-27): The shell beak of 
all three species is less distinct (Figure 4, drawings 22, 24, 
and 26). Shells have several features distinguishing each 
other. These include the beak lines (discussed under Stage 
III), number of whorls (Strombus gigas has 3 whorls, S. 
raninus has 4 whorls, and S. costatus has 3.5 whorls), shell 
length (Figure 3), and shape of the shell (S. gigas is round 
and squat [Figure 4, drawings 22 and 23], S. raninus is 
elongated [Figure 4, drawings 24 and 25], and S. costatus 
is elongated with a tilted apex [Figure 4, drawing 26]). 


Stage V (Figure 4, drawings 28-33): At competence the 
beaks of all species have disappeared and only Strombus 
gigas and S. costatus have traces of the beak lines remaining 
(Figure 4, drawings 28, 30, and 32). Sizes differ (Figure 
3), and spire shapes are very distinct. Strombus gigas has 
a rounded, squat spire (Figure 4, drawings 28 and 29); S. 
raninus has a triangular, pointed spire (Figure 4, drawings 
30 and 31); and S. costatus has an elongated spire with 
slightly concave sides (Figure 4, drawings 32 and 33). The 
number of whorls at competence also differs: S. gigas and 
S. costatus have 4 whorls, and §. raninus has 5 whorls. 
Strombus costatus and S. raninus shells become more trans- 
lucent by this stage, and the S. raninus shell has small 
pustulate markings. 


Sorting Plankton for Strombus Species 


Several key characteristics shared by these three Strom- 
bus species are used to identify them when sorting pre- 
served plankton. Under a dissecting microscope (20-40 x ) 
the purple-edged, wrinkled velar lobes, creamy white tis- 
sue, and black eye spots can be clearly recognized through 
the shell. Larval shells of these Strombus species have a 
long beak from hatching through day 10, at which time 
the beak becomes less distinct, vanishing completely by 
competence. A beak line can be seen on all species, but is 
most apparent on S. gigas shells. All three Strombus species 
hatch with two velar lobes, develop four lobes by day 5, 
and have six lobes by day 10. The lobes continue to elongate 
until the veliger becomes competent. 


DISCUSSION 


Larvae of Strombus gigas, S. costatus, and S. raninus can be 
clearly distinguished from each other with confidence at 
all stages. Although our descriptions are based upon lab- 
oratory cultures, we have sorted thousands of Strombus 
veligers taken in the Bahamas and Florida with no obvious 
differences in the morphology between wild and labora- 
tory-reared specimens. Therefore, we believe that the de- 
scriptions and illustrations in this study will be applicable 
in the entire Caribbean region. 

Field collections of Strombus veligers have been made in 
the eastern Caribbean Sea (POSADA & APPELDOORN, 1992), 
the Exuma Cays, Bahamas (CHAPLIN & SANDT, 1992; 
STONER et al., 1992a, b), and the Florida Keys (Stoner, 
unpublished data). Most of these collections were made 


M. Davis et al., 1993 


Page 243 


with 202-um-mesh plankton nets towed through approx- 
imately 200 m?* in near-surface water. This mesh size 
appears to be adequate for efficient collection of newly 
hatched S. gigas and S. costatus veligers, but surveys for 
smaller strombid veligers, such as those of S. raninus, will 
require a mesh size not exceeding 150 wm. This smaller 
mesh would increase considerably the time necessary for 
sorting. Densities as high as 2.0 S. gigas veligers/m? are 
known in areas around the Exuma Cays where repro- 
ductive stocks are high (Stoner, unpublished data). Tows 
made in the Exuma Cays during high wind periods fre- 
quently result in zero S. gigas and S. costatus veligers re- 
covered, even during peak larval season (Stoner, unpub- 
lished data). This may be related to sinking of veligers 
during periods of high turbulence; therefore, sampling dur- 
ing rough conditions should be avoided. 

Collections should be preserved in a buffered (pH = 
7.5-8.5) formalin-seawater mixture. The shells of newly 
hatched strombids are thin and important identification 
features (i.e., beaks, beak lines, and siphonal canals) are 
subject to relatively rapid loss by dissolution in acidic so- 
lutions. The heavier shells of late stage larvae are consid- 
erably more durable and easily preserved. With reasonable 
attention to preservation, even early stage Strombus veligers 
have been stored for periods exceeding two years without 
significant dissolution. 


Larval Dispersal Processes 


From routine laboratory and hatchery cultures of Strom- 
bus gigas and S. costatus larvae, growth rates and time to 
competence are known to vary with temperature, nutrition, 
and density of culture (BOIDRON-METAIRON, 1992; 
BROWNELL, 1977; Davis, 1992; GLAZER & BERG, 1992; 
M. Gongora, personal communication; L. Rodriguez-Gil, 
personal communication). For instance, the onset of com- 
petence for S. gigas larvae can occur between 16 and 28 
days, and S. costatus larvae can become competent as soon 
as 20 days and as late as 35 days. Strombus raninus larvae 
have not been cultured routinely; however, variations in 
the number of days to competence occurred in this study. 
Some larvae showed signs of competence at 38 days and 
others as late as 48 days, but the mean numbers of days 
to competence was 40. 

Our examination of larval development under uniform 
culture conditions permits a comparison of water-column 
mortality and long-distance dispersal in the three subject 
species. Strombus gigas should have the lowest water-col- 
umn mortality because of its rapid development and short 
larval life. On the other hand, the high fecundity of S. 
raninus may be an adaptation to long larval life and as- 
sociated high mortality rates during the planktonic phase. 
Widespread gene flow among Caribbean populations of 
S. gigas (MITTON et al., 1989; CAMPTON et al., 1992) could 
be related to the length of larval life and larval transport 
processes. In a typical Caribbean surface current of 0.2- 
0.5 m/sec (GRANT & WYATT, 1980; KINDER, 1983), an 


S. gigas veliger could be transported 43 km per day or 
about 900 km during the three-week larval period. Strom- 
bus costatus would be transported approximately 1400 km, 
and S. raninus approximately 1800 km, twice the distance 
of S. gigas. With these calculations, populations of S. gigas 
in the Florida Keys could have originated in spawning 
sites in Mexico or Cuba but could probably not have a 
source farther south or east in the Caribbean Sea. Strombus 
raninus larvae, however, could be transported across most 
distances in the Caribbean region. Precise knowledge of 
transport potential will depend upon new information on 
variations in developmental rates for wild larvae exposed 
to changes in nutrition, temperature, and salinity during 
their planktonic period, and on the ontogenic behavior of 
the veligers, particularly that related to vertical migration. 


ACKNOWLEDGMENTS 


This research was supported by a grant from the National 
Undersea Research Program, NOAA, U.S. Department 
of Commerce. We thank S. O’Connell and M. Ray for 
help in collecting egg masses and brood animals. We ap- 
preciate the egg mass that M. Gongora supplied us. K. 
Clark generously provided access to his computer video 
system for veliger measurements and initial drawings (sup- 
ported by NSF grant BIR8961326). We offer a special 
thanks to B. Bower-Dennis, who drew and detailed the 
finished larval shell and egg mass illustrations. K. Clark, 
P. Mikkelsen, R. Robertson, and two anonymous review- 
ers provided helpful comments on the manuscript. 


LITERATURE CITED 


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APPELDOORN, R. S. & D. L. BALLANTINE. 1983. Field release 
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APPELDOORN, R. S. & B. RODRIGUEZ (eds.). 1992. Queen Conch 
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BERG, C. J. 1976. Growth of the queen conch Strombus gigas, 
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BERG, C. J. & D. A. OLSEN. 1989. Conservation and man- 
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BoIDRON-METAIRON, I. 1992. A new approach to comparative 
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BROWNELL, W.N. 1977. Reproduction, laboratory culture, and 
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Campton, D. E., C. J. BerG, L. M. RosBison & R. A. GLAZER. 
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CHAPLIN, J. & V. J. SANDT. 1992. Vertical migration and 
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CLENCH, W. J. & R. T. Aspotr. 1941. The genus Strombus 
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D’Asaro, C. N. 1965. Organogenesis, development, and meta- 
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Davis, M. 1992. Mariculture techniques for queen conch 
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Davis, M. & R. C. HEsseE. 1983. Third world level conch 
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Davis, M., R. C. HEssE & G. A. HODGKINS. 1987. Commercial 
hatchery produced queen conch, Strombus gigas, seed for the 
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Davis, M., B. A. MITCHELL & J. L. Brown. 1984. Breeding 
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GLAZER, R. A. & C. J. BERG. 1992. Current and future queen 
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GRANT, C. J. & J. R. WyaTT. 1980. Surface currents in the 
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GUILLARD, R.R.L. 1975. Culture of phytoplankton for feeding 
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KINDER, T. H. 1983. Shallow currents in the Caribbean Sea 
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ers. Bulletin of Marine Science 33:239-246. 

MiTTON, J. B., C. J. BERG & K. S. Orr. 1989. Population 


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structure, larval dispersal, and gene flow in the queen conch, 
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356-362. 

MoscaTELL], R. 1987. The Superfamily Strombacea from 
Western Atlantic. Nano & Filho Ltda.: Brazil. 91 pp. 
PosaDA, J. & R. S. APPELDOORN. 1992. Preliminary obser- 
vations on the distribution of Strombus larvae in the eastern 
Caribbean. Jn: R. S. Appeldoorn & B. Rodriguez (eds.), 
Queen Conch Biology, Fisheries, and Mariculture. Fun- 

dacion Cientifica, Los Roques: Caracas, Venezuela. 

RANDALL, J. E. 1964. Contributions to the biology of the queen 
conch Strombus gigas. Bulletin of Marine Science 14:246- 
295: 

ROBERTSON, R. 1959. Observations on the spawn and veligers 
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Malacological Society of London 33:164-171. 

RODRIGUEZ-GIL, L. A., A. J. OGAWA & C. A. MARTINEZ- 
PaLacios. 1991. Hatching of the queen conch, Strombus 
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The Veliger 36(3):245-251 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Studies on the Reproduction and Gonadal 


Parasites of issurella pulchra 


(Gastropoda: Prosobranchia) 


by 


MARTA BRETOS anpD RICCARDO H. CHIHUAILAF 


Departamento de Ciencias Basicas, Facultad de Medicina, Universidad de La Frontera, 
Casilla 54-D, Temuco, Chile 


Abstract. 


Reproduction in the keyhole limpet Fissurella pulchra was studied at Huayquique, northern 


Chile, and the parasitism of its gonad by the digenean trematode Proctoeces humboldti was analyzed. 
The reproductive condition was assessed through the gonadosomatic index (GSI). Mean GSI showed 
two marked declines during the study period (in late autumn and in summer), suggesting the occurrence 
of two spawning periods per year. The F. pulchra population under study seems to be a partial spawning 
one, where the various size classes spawn at different seasons. Full reproductive potential seems to be 
attained at about 55 mm in shell length; thus, harvesting of individuals shorter than 60 mm (6 cm) in 
shell length for commercial or industrial purposes is not advisable. The prevalence and mean intensity 
of infection by Proctoeces increase with the size of the limpet hosts. The prevalence of infection did not 
differ between females and males, nor did the percentages of infection vary among monthly samples 


through the collecting period. 


INTRODUCTION 


The largest keyhole limpets of the genus Fissurella live on 
Chilean coasts. During the past 15 years, these gastropod 
mollusks have progressively attracted research workers’ 
attention, particularly after Bretos reported the presence 
of adult digenea trematodes parasitizing the gonads of 
Fissurella (BRETOS & JIRON, 1980). This finding suggests 
that these mollusks are the definitive hosts for trematodes 
of the genus Proctoeces. 

Fissurella pulchra Sowerby, 1835, is a rare species of the 
genus. It is restricted to certain habitats, where its popu- 
lations seem to have low density. Biological studies on it 
are limited to taxonomy (MCLEAN, 1984), biometry, hab- 
itat and epibiotic organisms fixed on the shell (BRETOS & 
CHIHUAILAF, 1990), and the finding that trematodes occur 
in 77.5% of the specimens analyzed in northern Chile 
(BRETOS & JIRON, 1980). Fissurella pulchra can be found 
from Salaverry, Peru (8°14’S) to Rio Bio-Bio, Concepcion 
Province, Chile (36°48’S) (MCLEAN, 1984). McLean de- 
tected only small individuals at most Peruvian localities; 
the largest were living in central Chile. 

In spite of the scarce knowledge of Fissurella pulchra, it 
has been exploited as food, together with other limpets in 
Chile (BRETOs, 1988), at Coquimbo, Iquique, San An- 


tonio, and Talcahuano. Consequently, it is important to 
study such basic aspects of its life cycle as reproduction 
and growth. 

The aim of this paper is to present aspects of the re- 
production and occurrence of the trematode Proctoeces 
humboldt: George-Nascimento & Quiroga, 1983, in the 
gonads of Fissurella pulchra in northern Chile. 


MATERIALS anp METHODS 


Random samples of Fissurella pulchra were taken at 
Huayquique (20°17'S, 70°8’W) every two months from 
April 1979 to May 1980. Collections were made from 
rocky substrates by diving in shallow waters, from 1.5 to 
3 m below the low-water mark. Sampling covered the 
available size range. 

Shell length was measured to 0.1 mm, and body and 
gonad wet weight to 0.1 g. The sex of each limpet was 
determined by dissection. The hypothesis of equal repre- 
sentation of both sexes in the Fissurella pulchra population 
under study was tested. Chi-square was calculated by using 
the correction for continuity of Yates (ZAR, 1984). The 
trematodes found in the ovary and testes were counted. 

Length data were grouped in size classes of 5 mm each. 
The reproductive condition for each individual was eval- 


Page 246 


Table 1 


Examined material of Fissurella pulchra from Huay- 

quique. n = number of females or males; % = percentage 

of sexes; M = percentage of animals estimated as ripe; 
Und = sexually undetermined specimens. 


Sexed animals 


Females Males 

Date n % M n % M_ Und Total 
Apr. ’79 37 60.6 44.4 DAS3 9 ASO ler 1 62 
Jun. °79 19 47.5 0 Pil BA5) 5.0 0) 40 
Sep. °79 16 33.3 28.6 32 66.7 60.0 1 49 
Nov. ’79 24 48.9 75.0 25, 5 92:0 (0) 49 
Jan. ’80 27 58.6 46.2 19 41.4 66.7 3 49 
Mar. ’80 15 30.0 0) 35 eOLOR lial 2; by 
May ’80 24 55.8 17.4 19 44.2 44.4 4 47 

Total 162 175 11 348 


uated on the basis of a gonadosomatic index (GSI), and 
on the gonadal characteristics. GSI was calculated by ex- 
pressing the ratio of gonad weight to the total soft-part 
weight as a percentage. Monthly GSI means were cal- 
culated for each sex. Sexual maturity of each animal was 
estimated by considering its GSI and the size and ap- 
pearance of the gonad (BRETOS et al., 1983). A table with 
minimum GSI values per size class was made, to classify 
each animal as sexually mature if it had a GSI equal to 
or higher than minimal GSI. The minimum GSI was 
arbitrarily calculated by adding a one to the mean GSI in 
each size class divided by two, using samples where most 
of the animals collected presented high GSI values. 

The prevalence and intensity of infection by trematodes 
were analyzed in sexed Fissurella pulchra of all sizes classes. 
Statistical tests applied to this analysis were performed 
following the methodology recommended by Zar (1984), 
and the significance level of a = 0.05 was chosen. Para- 
sitologic terms used are those recognized by MARGOLIS et 
al. (1982). 

Surface seawater temperature was recorded at 08:30 hr 
(minimum temperature) in the sampling site during the 
study period, and monthly mean values were calculated. 


RESULTS 


Among the 348 Fissurella pulchra individuals collected, 162 
were females, 175 were males, and 11 were juveniles of 
undetermined sex (Table 1). The population of F. pulchra 
was not large enough to allow collection of larger and more 
frequent samples. 

Females measured from 26.8 to 64.7 mm in shell length, 
males from 27.5 to 63.5 mm, and juveniles from 24.8 mm 
to 53.3 mm. Mean size in females was 47.48 mm (SD + 
8.43 mm) in shell length and 48.52 mm (SD + 7.32 mm) 
in males in the whole sample of Fissurella pulchra. There 
was no significant difference between these mean values 


The Veliger, Vol. 36, No. 3 


25 
G 
N 
A 1.55 2 
M 
E 
A 
N alla 
WwW 
i 
G 
6 0.5- Z 
T 
9g 
O+ T T = T T T T T 71 
25 30 35 40 45 50 55 60 65 70 


SHELL LENGTH mm 
Figure 1 


Mean values of gonad wet weight per size class in Fissurella 
pulchra from Huayquique. 


(Student’s test, ¢ = 0.976; P = 0.329). As was shown by 
variance analysis, mean shell lengths in monthly samples 
were significantly different (F = 6.063; P < 0.001). 


Sexes and Gonads 


Fissurella pulchra has separate sexes. No signs of her- 
maphroditism or sex change were detected at any shell 
length. 

Sex cannot be discerned from external features in these 
keyhole limpets, only from direct examination of the un- 
paired gonad. Sexually undetermined juveniles have a small 
or undetectable gonad, which is translucent or whitish in 
color. Ovaries are green, and testes are pale yellow, varying 
to beige. Morphological characters of the gonads in Fis- 
surella pulchra are similar to those previously described for 
F. maxima (BRETOS et al., 1983). 

The mean weight of gonads in the whole sample (Figure 
1) increased until the 50-55 mm shell length size group. 
No significant growth occurred over this size. The mature 
ovary attained a wet weight of 4.0 g, and the mature testes 
3.1 g in the population under study. 


Sex Ratios 


Of the sexed animals, 48.1% were females and 51.9% 
were males, giving a sex ratio of 1:1 in the population 
examined (x? = 0.427; P = 0.513). 

The proportions of sexes in specimens of all lengths are 
constant (Figure 2), supporting the conclusion that sex 
reversal is absent in the species. Some significantly differ- 
ent sex ratios were observed in some months (Table 1). 
Males were more numerous in September and March, 
while females predominated in April, January, and May. 


Reproductive Condition 


A GSI value was used to assess the reproductive activity 
of each limpet. The assumption is that an increase in GSI 


M. Bretos & R. H. Chihuailaf, 1993 


165 


145 


<mn 


—— Undet. 


125 3 Males 


105 
85 
65 


—— Females 


4- 
24 
0+ 


25 30 35 40 45 50 55 60 £465 
SHELL LENGTH mm 


X Z2ZO-ACW—-DAH-O 


I T T 


Figure 2 


Percentages of sexes per size class in Fissurella pulchra collected 
at Huayquique. 


correlates with a build-up of gametogenic cells, while a 
decrease indicates spawning. 

Mainly on the basis of its GSI, each animal was clas- 
sified as “ripe” or “spent.” Limpets with spent and re- 
covering gonads were classed together as spent individuals; 
specimens with high GSI values were considered as sex- 
ually mature or ripe. Table 1 shows the sexual maturity 
estimates for both sexes in each sample. Many females 
were mature in April, November, and January, while 
mature males were also numerous in September. Mature 
males were present in all samples examined. 

The smallest female estimated as sexually mature was 
30.1 mm in shell length, and the smallest male measured 
30.2 mm. However, the minimum size at which sexual 
maturity is attained by the studied population could not 
be determined, because insufficient quantities of specimens 
were in each analyzed sample. Many individuals of Fis- 
surella pulchra classified as sexually mature (Table 1) oc- 
curred in April and in November. No mature females were 
detected in June or in March, and mature males also were 
scarce in these months. 

Monthly mean GSI values varied throughout the year 
(Figure 3). GSI variations in both sexes followed the same 
tendency, although the mean GSI in males always showed 
higher values than those in females. 

The relationship between GSI and size in samples with 
the highest GSI values (Figure 4) shows that GSI increases 
as the animal grows until 55 mm in shell length; over this 
size GSI declines. 


Spawning 


The lowest values of monthly mean GSI (Figure 3) 
were found in June 1979 and in March 1980, meaning 
that animals had spent gonads at these dates. The estimates 
of sexual maturity (Table 1) showed a sharp decrease in 
the same samples. These findings suggest that the Frssurella 
pulchra population has finished a reproductive period in 
June and in March. Spawning probably occurred in May— 


Page 247 


165 18 


zPmz 
mpca>oUmvema 


-oD 


Figure 3 


Variations in mean gonadosomatic index per sample in Fissurella 
pulchra, and mean minimal temperatures of the surface seawater 
at Huayquique. Squares: GSI of males; diamonds: GSI of fe- 
males. Arrows show presumable spawning periods. 


June (late autumn) and between December and February 
(summer). 

A decrease in seawater temperatures coincides with the 
spawning period of late autumn (arrow in Figure 3), and 
the highest temperatures of the year coincide with the 
summer spawning period. These facts seem to support a 
relationship between fluctuations in seawater temperature 
and gamete release. 

The detection of more than one spawning period per 
year could have been due to different age classes (size 
classes) releasing their gametes at different seasons. For 
this reason, mean GSI per size class was analyzed for each 
sample. Horizontal lines (Figure 5) were drawn to mark 
the minimum GSI to be considered as ripe in each class. 
The oldest animals collected (over 60 mm in shell length) 
were ripe in January (Figure 5e), spawning probably in 
summer. The youngest specimens (30-40 mm) seemed to 
spawn in spring (Figure 5c, d, e). The median size classes 


115 


zPme 


4+ T 


20 30 40 50 60 70 80 
SHELL LENGTH mm 


Figure 4 


Mean gonadosomatic index for size class of Fissurella pulchra 
collected in April and November (n = 109) at Huayquique. 


Page 248 The Veliger, Vol. 36, No. 


105 105 
a e 
87 8-4 
M M 
A 64 E 6. 
N N 
| 
G | 4 
ane iS 4 
1 1 
oe 24 
Tz T T T T T (0) T T T T 
27.5 325 37.5 425 47.5 525 57.5 62.5 27.5 325 37.5 425 47.5 525 57.5 62.5 
10> 10> 
b f 
85 8° 
F 6 A 64 
N N 
a a4 
1 1 
24 2 - 
0 T = tae T T 0 T T T T 
27.5 325 37.5 425 47.5 525 57.5 62.5 27.5 32.5 37.5 425 475 525 57.5 62.5 
10> 105 
Cc 
8 - g 
84 
M M 
E 
6+ E | 
nN vie 
G 4 J 
Shoe gS 4 
! 1 
24 24 
0 : : : ES : 0 8 d a: : EE 
27.5 32.5 37.5 425 47.5 525 57.5 62.5 27.65 325 37.5 42.5 475 525 57.5 62.5 
SHELL LENGTH mm 
10) 
d aa 
8-5 
M 
A 67 
N 
G 4 
$ 4 
1 
24 
27.5 32.5 375 425 475 525 57.5 62.5 
Figure 5 


Mean gonadosomatic index (GSI) per size class of Fissurella pulchra in each monthly sample (empty bars) and 
minimal GSI to be estimated sexually mature in each size group (black bars). a. April 1979. b. June 1979. c. 
September 1979. d. November 1979. e. January 1980. f. March 1980. g. May 1980. 


M. Bretos & R. H. Chihuailaf, 1993 


appeared to spawn in late autumn (Figure 5a, b) and late 
spring (Figure 5d, e). 


Parasites in the Gonads 


The prevalence of infection by Protoeces humboldti was 
83.38% among the sexed Fissurella pulchra examined, 85.5% 
among females and 81.1% among males. There were no 
significant differences between the prevalence in the two 
sexes (G = 0.003; P = 0.316). Only two sexually unde- 
termined specimens were parasitized, one of them had one 
trematode and the other had three. 

The prevalence of infection (using angular transfor- 
mation) in size classes increased with increasing shell length 
(Figure 6; 7 = 0.89; P > 0.02; n = 8). All limpets over 
55 mm in shell length were parasitized. There was a high 
exponential correlation between the mean intensity of in- 
fection and the size of Fissurella pulchra (r = 0.934; P < 
0.001; n = 8) (Figure 6). 

The prevalence of infection, evaluated using a contin- 
gency table, showed little variation throughout the year, 
and there were no significant differences among the per- 
centages of infection of monthly samples (x? = 0.89; P = 
0.96). Variations in the prevalence of infection through 
the seasons had no correlation to mean size per sample (7 
= 0.01; P= 0.92; n = 7). 

The smallest infected female was 26.8 mm long, while 
the smallest infected male was 27.5 mm long. The mean 
intensity of infection in sexed animals was 5.92 (SD + 
5.23) trematodes per keyhole limpet host. Infection inten- 
sity in females ranged from 1 to 42 (in a 62.1 mm female) 
parasites per host (mean 6.54 + 5.98), and it fluctuated 
in males from 1 to 22 (in a 58.1 mm male) (mean 5.38 + 
4.30). Mann-Whitney tests revealed no significant differ- 
ences (Z = 1.59; P > 0.05) in mean intensity for the two 
Sexes. 

The mean intensity of infection displayed small fluc- 
tuations during the study period. Peaks in mean intensity 
were observed in September, January, and May, while 
the lowest values occurred in November and March. Vari- 
ations in mean intensity through the seasons were corre- 
lated to mean size per sample (7 = 0.681; P = 0.09; n = 
De 


DISCUSSION 


In Fissurella species, sex can be determined for individuals 
of sizes 26-28 mm (BRETOS et al., 1983, 1988a). In spite 
of this, sexually undetermined individuals have been de- 
tected over 53 mm in F. pulchra and F. picta, and up to 
72 mm in F. maxima. In the last species it was assumed 
that gonad development was retarded by the high preva- 
lence (73.7%) of trematodes found in juvenile gonads, which 
presented an intensity of infection ranging up to 17 par- 
asites per host (BRETOS et al., 1983). Only a few individuals 
of undetermined sex were found in collected samples of F. 
picta and F. pulchra, and they were sparsely parasitized. 
This fact suggests that in the analyzed populations of these 


Page 249 
, 20 
E 
Ae 
5 15 A 
R 
E 
M4 1 
tS +10 N 
N 
fi 40+ E 
N 
< s 
E L 5 1 
20 4 y 
O-+ aT T T Tas T 0 


25 30 35 40 45 SO 55 60 65 
SHELL LENGTH mm 


Figure 6 


Prevalence of infection (black squares) and mean intensity (open 
triangles) per size class in Fissurella pulchra. 


last two species, gonadal development may be mainly de- 
termined by individual variability and other endogenous 
factors. 

Although hermaphroditism or change of sex has been 
mentioned for Fissurella (BAccI, 1947) or for Haliotis 
(GIRARD, 1972), these phenomena have not been observed 
in Chilean fissurellids (BRETOS eft al., 1983, 1988a, b; 
Osorio et al., 1986). The sex ratio is 1:1 in F. pulchra 
from Huayquique, the same as in F. nigra (BRETOS et al., 
1988b), in F. picta (BRETOS et al., 1988a), and in F. maxima 
from Huayquique (BRETOS ef al., 1983) and from Los 
Vilos (Osorio et al., 1986). Occasionally, an archaeogas- 
tropod may show a disparity of sexes, as has been observed 
in F. barbadensis, a small-sized Caribbean species (WARD, 
1966) or in some Haliotis species (SHEPHERD & LAws, 
1974). 

In Fissurella pulchra the mean GSI increases until 55 
mm in shell length (Figure 4), diminishing at greater sizes. 
The same tendency has been shown to occur in the abalone 
Haliotis midae (NEWMAN, 1967), in a relationship between 
gonad bulk index (equivalent to GSI) and size. This seems 
to indicate that the gonads attain their maximum devel- 
opment (z.e., their full reproductive potential), at sizes 
around 55 mm in F. pulchra. Longer individuals have 
reduced reproductive potential. Based on these consider- 
ations, it appears not advisable to catch F. pulchra speci- 
mens shorter than 60 mm in shell length for commercial 
or industrial purposes. 

The Fissurella pulchra population under study seems to 
demonstrate partial spawning, where the various size class- 
es spawn at different seasons, but the population as a whole 
shows two main spawning periods per year (Figure 3). 
These periods are explained by the release of gametes of 
median and large-sized animals. The spawning of small 
individuals (up to 40 mm) seems to be of low intensity, 
and does not have significance to the population. 

Reproductive data are available for some other Chilean 
Fissurella species. Variations in GSI suggest that F. maxima 


Page 250 


presents two spawning periods per year: the main in late 
spring-early summer, and a secondary period in winter, 
at Huayquique, northern Chile (BRETOS ef al., 1983). 
Studies conducted at Queule and Cheuque, in southern 
Chile, have shown a similar spawning pattern for F. nigra 
(in late summer, and winter) (BRETOS et al., 1988b) and 
for F. picta (in late summer, and in spring) (BRETOS et al., 
1988a). In all these species, animals considered to be ripe 
were present throughout the year, although they were 
scarce or absent in some months. 

Fissurella barbadensis from the coasts of Barbados pre- 
sents two principal spawning periods (WARD, 1966): from 
September to November and from March to June. His- 
tological analysis also showed spawning specimens in all 
except two samples. These findings agree with those ob- 
tained for Chilean keyhole limpets. Partial spawning has 
not been investigated in those species. 

Concholepas concholepas, a Chilean gastropod, also pre- 
sents more than one spawning period per year at Caleta 
Hornos (29°38'S, 71°20'W) according to variations ob- 
served in the population mean GSI (LozaDa et al., 1989). 
The highest GSI values occurred in January and in April- 
May, where all size groups were spawning (70-110 mm). 
Nevertheless, different reproductive behavior was detected 
among widely different size groups. 

The prevalence of trematodes in the gonads of Fissurella 
species is highly variable, from 13.97% in F. crassa to 
96.97% in F. maxima (BRETOS & JIRON, 1980). The prev- 
alence of Protoeces humboldti was nearly constant in F. 
pulchra during the study period. The same has been ob- 
served in Batillus cornutus infected by P. ichthara: (SHIMURA, 
1980), or in Nucella lapillus by P. maculatus (PONDICK, 
1983). These findings could be related to a long adult life- 
span of the parasite, as in the case of P. ichihara: (SHIMURA, 
1980). No seasonal influence on the prevalence of infection 
by Proctoeces in F. maxima from Los Vilos (OsorRIO et al., 
1986) or in F. crassa from Antofagasta (OLIVA & Diaz, 
1988) has been demonstrated. 

The prevalence of infection by Proctoeces is influenced 
by the host’s locality. Different prevalences have been de- 
tected in Fissurella crassa from Iquique (13.97%) (BRETOS 
& JIRON, 1980) or Antofagasta (80.4%) (OLIVA & Diaz, 
1988). A similar occurrence was reported by PONDICK 
(1983), in which the intertidal snail Nucella lapillus from 
two sites of the same beach presented different percentages 
(0% and 4.7%) of infection by P. maculatus. The dissimilar 
prevalences of the same parasite in the same hosts could 
be attributed to the diverse ecological conditions in the 
habitats (microhabitats) occupied by these gastropods at 
those geographical places. 

The prevalence of infection by Proctoeces humboldti in- 
creases with the size of the host in Fissurella pulchra (this 
study) and in F. crassa from Antofagasta (OLIVA & Diaz, 
1988). In F. maxima from Los Vilos (Osorio et al., 1986) 
prevalence reaches its highest values in median-sized in- 
dividuals, decreases in larger animals, and is absent in the 
oldest specimens. Osorio et al. (1986) assumed that the 


The Veliger, Vol. 36, No. 3 


lower prevalence presented by large-sized limpets was due 
to their living in deeper habitats, removed from infecting 
larvae. 

The relationship between mean intensity of infection 
and the size of hosts varies from one species to another. 
Data reported for Frssurella maxima from Los Vilos suggest 
that there is no relation between these two variables. In 
F. crassa from Antofagasta, intensity is directly correlated 
to host length, while in F. pulchra, we have found an 
exponential relationship between mean intensity of infec- 
tion and the shell length of the hosts. 

Although OLIvA & Diaz (1988) stated that there are 
significant differences in the mean intensity of infection 
according to host sex, we have not detected differences 
between females and males. 

Further studies on Proctoeces humboldti will be needed 
to understand its relations with Fissurella species. Among 
these are the elucidation of the life cycle and life-span of 
this parasite, and the identification of the conditions re- 
quired for infecting the keyhole limpets. 


LITERATURE CITED 


Baccl, G. 1947. Osservazioni sulla sessualita degli Archaeo- 
gastropoda. Archivio Zoologico Italiano 32:329-341. 

BreTos, M. 1988. Pesqueria de lapas en Chile. Medio Am- 
biente 9(2):7-12. 

Bretos, M. & R. H. CuHInualLar. 1990. Biometria y otros 
aspectos biologicos de Fissurella pulchra (Mollusca: Proso- 
branchia). Revista de Biologia Marina, Valparaiso 25(1):1- 
14. 

BreETos, M., J. GUTIERREZ & Z. ESPINOZA. 1988a. Estudios 
biologicos para el manejo de Fissurella picta. Medio Ambiente 
9(1):28-34. 

BreTos, M. & C. JIRON. 1980. Trematodes in Chilean Fis- 
surellid molluscs. The Veliger 22:293. 

BreETOos, M., V. QUINTANA & V. IBARROLA. 1988b. Bases biol- 
ogicas para el manejo de Fissurella nigra. Medio Ambiente 
9(1):55-62. 

BreTos, M., I. TESORIERI & L. ALVAREZ. 1983. The biology 
of Fissurella maxima Sowerby (Mollusca: Archaeogastropo- 
da) in northern Chile. 2. Notes on its reproduction. Biological 
Bulletin 165:559-568. 

GEORGE-NASCIMENTO, M. & G. QurRoGA. 1983. Descripcion 
de una nueva especie de trematodo, Proctoeces humboldti n. 
sp. (Digenea: Fellodistomidae) parasito de las lapas Fissu- 
rella spp. Bruguiére, 1789 (Mollusca: Archaeogastropoda). 
Parasitologia al Dia 7:100-103. 

GiesE, A. C. & J. S. PEARSE. 1974. Introduction: general prin- 
ciples. Pp. 1-49. In: A. C. Giese & J. S. Pearse (eds.), 
Reproduction of Marine Invertebrates. Vol. I. Academic 
Press: New York. 

GIRARD, A. 1972. La réproduction de ’ormeau, Halvotis tuber- 
culata L. Revue des travaux. Institut des Péches Maritimes, 
Nantes 36:163-184. 

Lozapa, E., P. CANAS & M. R. SCHUFFENEGER. 1989. Ciclo 
reproductivo del recurso loco (Concholepas concholepas). Pp. 
14-39. In: Estudio de Repoblamiento de Recursos Benton- 
icos, Area Piloto IV Region. Vol. II. Ed. CORFO-IFOP. 

Marco1ls, L., G. W. Esco, J. C. HOLMEs, A. M. Kuris & G. 
A.SCHAD. 1982. The use of ecological terms in parasitology 
(Report of an ad hoc Committee of the American Society of 
Parasitologists). Journal of Parasitology 68(1):131-133. 


M. Bretos & R. H. Chihuailaf, 1993 


McLean, J. H. 1984. Systematics of Fissurella in the Peruvian 
and Magellanic faunal provinces (Gastropoda: Prosobran- 
chia). Natural History Museum, Los Angeles County, Con- 
tributions in Science, No. 354. 70 pp. 

NewMan, G. G. 1967. Reproduction of the South African 
abalone Haliotis midae. Division of Sea Fisheries Investi- 
gational Report No. 64. 24 pp. Cape Town. 

Outiva, M. & M. Diaz. 1988. Aspectos cuantitativos de la 
infeccion por Proctoeces humboldti (Trematoda: Fellodistom- 
idae) en la lapa Fissurella crassa (Mollusca: Archaeogastropo- 
da). Revista Chilena de Historia Natural 61:27-33. 

Osorio, C., H. Diaz & M. Rios. 1986. Prevalencia de Proc- 
toeces humboldti George-Nascimiento y Quiroga, 1983 (Di- 
genea, Fellodistomidae) en la poblacion de Fissurella maxima 
Sowerby, 1835 (Mollusca: Archaeogastropoda) de Los Vilos, 
en Chile. Revista de Biologia Marina, Valparaiso 22(2): 
157-168. 

Ponpick, J.S. 1983. The geographical distribution of an adult 


Page 251 


trematode, Proctoeces maculatus, in the gastropod Nucella la- 
pilus from New England. Proceedings of the Helmintho- 
logical Society of Washington 50(1):174-176. 

SHEPHERD, S. A. & H. M. Laws. 1974. Studies on southern 
Australian abalone (genus Haliotis). II. Reproduction of five 
species. Australian Journal of Marine and Freshwater Re- 
search 25:49-62. 

SHIMURA, S. 1980. Ecological aspects of Proctoeces ichiharai 
(Trematoda: Digenea) parasitic in Batillus cornutus (Gas- 
tropoda). Marine Ecology Progress Series 3:145-149. 

WarD, J. 1966. The breeding cycle of the keyhole limpet Fis- 
surella barbadensis Gmelin. Bulletin of Marine Sciences, Gulf 
Caribbean 16:685-695. 

WEBBER, H. H. 1977. Gastropoda: Prosobranchia. Pp. 1-98. 
In: A. C. Giese & J. S. Pearse (eds.), Reproduction of Marine 
Invertebrates. Vol. IV. Academic Press: New York. 

ZAR, J. 1984. Biostatistical Analysis. Prentice Hall Inc.: New 
York. 718 pp. 


The Veliger 36(3):252-258 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Genital Dimorphism in the Land Snail 
Chondrina avenacea: Frequency of Aphally in 
Natural Populations and Morph-specific 
Allocation to Reproductive Organs 
by 


BRUNO BAUR anD XIAOFENG CHEN 


Institute of Zoology, University of Basel, Rheinsprung 9, CH-4051 Basel, Switzerland 


Abstract. Several species of simultaneously hermaphroditic land snails show a genital dimorphism: 
aphallic individuals differ from euphallic ones by a lack of male copulatory organs (penis and genital 
retractor muscle). Aphallic individuals can self-fertilize or outcross as females but not as males. Thus, 
the mating system of a population may be significantly influenced by the proportion of aphallic indi- 
viduals. 

We present data on the frequency of aphally in 21 natural populations of the rock-dwelling land 
snail Chondrina avenacea in the surroundings of Basel, Switzerland. The populations varied greatly in 
percentage of aphallic individuals, ranging from 0.9 to 89.2% (grand mean 41.2%). This variation did 
not follow any discernible geographical pattern. The proportion of aphallic snails within a population 
was influenced neither by local population density nor by any other habitat characteristics (exposure 
of rock face, altitude of locality, number of other snail species present). 

The populations varied significantly in adult shell size. Within populations, aphallic individuals 
tended to be smaller than euphallic ones. After controlling for size differences, the reproductive organs 
amounted to 28.3% of the total body mass in aphallic snails and to 31.7% in euphallic snails in a 
population. This difference can be explained by the absence/presence of male copulatory organs, whose 
dry weight was 3.2% of the total body mass of euphallic individuals. Monthly sampling of snails from 
one population revealed that individuals of Chondrina avenacea did not change their sex type over the 


course of one year. 


INTRODUCTION 


Different reproductive systems have evolved in hermaph- 
rodites that allow different individuals within a population 
to reproduce either by self-fertilization or by outcrossing 
(e.g., gynodioecy in plants; GoUYON & COUVET, 1987). 
Aphally may be a comparable feature in hermaphroditic 
snails. Whereas the reproductive structure of snails usually 
consists of one hermaphrodite gonad and of male and fe- 
male ducts with accessory glands (= euphallic snails), 
aphallic individuals lack the male copulatory organs 
(Tompa, 1984). Aphallic snails can self-fertilize or out- 
cross as female, but not as male, whereas euphallic indi- 
viduals can outcross and self-fertilize (POKRYSZKO, 1987, 
1990). Thus, the mating system of a population may be 


significantly influenced by the ratio of aphallic to euphallic 
individuals. 

Aphally has been reported from numerous species of 
freshwater and terrestrial gastropods (WATSON, 1923; 
Tompa, 1984; POKRYSZKO, 1987) and has received most 
attention in the freshwater snail Bulinus truncatus (con- 
tortus) (Audouin) (LARAMBERGUE, 1939; JARNE & DELAY, 
1991; JARNE et al., 1992; SCHRAG et al., 1992). Pure aphal- 
lic, pure euphallic, and mixed populations occur in this 
species. In the rock-dwelling land snail Chondrina clienta 
(Westerlund), the frequency of aphally varied from 52.2 
to 99.1% in 23 natural populations on the Baltic island of 
Oland, Sweden (BAUR et al., 1993). Breeding experiments 
have revealed that both genetic and nongenetic components 
may influence the proportion of aphallic offspring in a 


B. Baur & X. Chen, 1993 


Page 253 


population. (LARAMBERGUE, 1939; SCHRAG et al., 1992; 
BAUR et al., 1993). Recently, SCHRAG & READ (1992) 
provided experimental evidence for a temperature-sensi- 
tive phally determination during the egg and hatchling 
stage in two populations of Bulinus truncatus. 

Sex allocation theory predicts that aphallic snails can 
invest more in gametes than euphallic ones because they 
have no cost related to the building and maintenance of 
male organs, if one assumes that both types of snails invest 
the same amount of energy in growth and survival (HEATH, 
1977; CHARNOV, 1982). This prediction presupposes that 
aphallic individuals do not adjust their female reproductive 
organs (albumen gland, female duct) to increase egg pro- 
duction. 

This paper examines aphally and sex allocation in the 
rock-dwelling land snail Chondrina avenacea (Bruguiére) 
in the surroundings of Basel (Switzerland). In particular, 
the following questions were addressed: (1) how frequently 
do aphallic individuals occur in natural populations of C. 
avenacea? (2) Is the frequency of aphally associated with 
any habitat characteristics, local population density and/ 
or snail size? (3) Do aphallic individuals have reduced 
fixed costs to build-up their reproductive organs compared 
with euphallic ones? And (4) is there any seasonal vari- 
ation in the frequency of aphallic individuals within a 
population (z.e., do individuals of C. avenacea change their 
sex type over the course of a year)? 


MATERIALS anp METHODS 
Species 


Chondrina avenacea occurs on rock faces and walls in 
limestone areas of western Europe and the Alps, attaining 
altitudes of 2000 m (KERNEY & CAMERON, 1979; 
GITTENBERGER, 1984). Chondrina avenacea has determi- 
nate growth; its cylindro-conical shell is dextral and in 
adults is 6 to 8 mm high (GITTENBERGER, 1973; NEUCKEL, 
1981). In northwestern Switzerland, C. avenacea co-occurs 
with Clausilia parvula Ferussac and Pyramidula rupestris 
(Draparnaud) on calcareous rock faces. Chondrina avena- 
cea is very resistant to drought (NEUCKEL, 1981). The 
snails’ specialized radula enables them to graze epi- and 
endolithic lichens growing on rock faces (SCHMID, 1929; 
BREURE & GITTENBERGER, 1982; BAUR et al., 1992). The 
snails are active during periods of high air humidity. Dur- 
ing winter (November-March) they are active only under 
mild conditions (warm rains); otherwise, they hibernate 
in small fissures or attached to the exposed rock surface 
(NEUCKEL, 1981; BAUR & Baur, 1991). Dispersal of 
marked C. avenacea on a rock wall (population 16; see 
below) averaged 234 cm in three months, the maximum 
distance recorded being 746 cm (B. Baur & A. Baur, 
unpublished data). Little is known concerning the life his- 
tory of C. avenacea. Preliminary results indicate that in- 
dividuals complete their shell growth at an age of 3-5 
years. Adult snails live 2-10 years (B. Baur, unpublished 
data). 


Sampling 


Specimens of Chondrina avenacea were collected on ver- 
tical rock walls ranging in height from 2 to 60 m in the 
surroundings of Basel, northwestern Switzerland (47°30'N, 
7°40'E), between July and October 1991. Samples con- 
sisting on average of 101 (range 65-117) fully grown C. 
avenacea were collected from areas of 4.5—24 m? (mean = 
10.9 m?) at each of 20 localities (for convenience referred 
to as populations) (Figure 1). Localities were situated at 
least 750 m apart from each other (in most cases several 
kilometers). At an additional locality (population 21: an 
isolated, 7 m long and 2-4 m high rock wall), samples 
consisting of 21-28 snails (mean = 22.8) were collected at 
monthly intervals from April 1991 to March 1992. 

At each locality the following variables were recorded: 
altitude (in meters above sea level), exposure of the rock 
face (degrees from south), number of other snail species 
present on the same face, area to which sampling was 
restricted (in m?), and local population density of Chon- 
drina avenacea. Snail density was estimated by counting 
the number of adults picked up with a pair of tweezers 
within 3 min by one of us (BB). Density estimates were 
based on 3-4 replicates (mean = 3.2) at each locality. A 
second estimate of local population density was obtained 
by relating the number of snails collected within 3 min to 
the sampling area (number of snails per 3 min and m’). 


Measurements 


The snails were frozen at —20°C. The size (total shell 
height) of each individual was measured to the nearest 
1/24 mm using a binocular microscope with a stage mi- 
crometer (a previous study revealed that most of the in- 
terpopulational variation in shell size of Chondrina clienta 
can be expressed by the single character of shell height 
(Baur, 1988)). The animals were dissected to determine 
their genital morph (aphallic or euphallic). Both sex types 
are illustrated by GITTENBERGER (1973). 

To evaluate differences in allocation to reproductive 
organs in aphallic and euphallic individuals and any sea- 
sonal changes in the allocation pattern, the genitals of snails 
from population 21 were separated from the soft body 
under a dissecting microscope. In euphallic individuals, 
the male copulatory organs (penis, epiphallus, penis re- 
tractor muscle) were also separated from the remaining 
parts of the reproductive organs (albumen gland, sperm- 
oviduct, female duct). The dry weight of the soft body, 
male copulatory organs (if present) and remaining genitals 
were determined (after drying for 48 hr at 100°C) using 
a Mettler AE163 balance (accuracy 0.01 mg). 


Statistical Analysis 


Data analysis was performed using the SAS program 
package (SAS INsTITUTE INC., 1989). Among-population 
differences in the proportion of aphallic snails were eval- 
uated using chi-squared tests. Correlation analysis was 


Page 254 


Figure 1 


Frequencies of aphallic and euphallic individuals in natural pop- 
ulations of Chondrina avenacea in the surroundings of Basel, Swit- 
zerland. Open sections refer to aphallic individuals and solid 
sections to euphallic individuals. Sample size for each population 
is given in Table 1. Stippled area indicates the city of Basel. 


used to examine any possible association between fre- 
quency of aphallic snails and local population density and 
altitude of the locality. Frequency data were arcsine-trans- 
formed. Possible influences of the exposure of rock faces 
and the number of co-existing snail species on the per- 
centage of aphallic Chondrina avenacea were evaluated by 
analysis of variance (ANOVA). Students ¢-tests were used 
to examine differences in body mass and reproductive or- 
gans between aphallic and euphallic individuals. 


RESULTS 
Variation in Aphally Among Populations 


The populations varied greatly in the frequency of 
aphallic individuals, but this variation did not follow any 
general geographical pattern (Figure 1). On average 41.2% 
of the snails were aphallic; the among-population variation 
ranged from 0.9 to 89.2% (Table 1). In most cases, pop- 
ulations situated 750 m from each other differed signifi- 
cantly in the percentage of aphallic individuals. However, 
there were two groups, each of three neighbor populations, 
in which the three populations did not differ in the pro- 
portion of aphallic individuals (populations 8, 9, and 10: 
x? = 3:08, di = 2, P > 0:2; populations 11h 12) andi 13: 


The Veliger, Vol. 36, No. 3 


x? = 1.23, df = 2, P > 0.4; Table 1, Figure 1). These 
neighbor populations were also isolated from each other; 
for example, populations 11 and 12 were separated by a 
distance of 2.1 km with a 170-m deep valley and a 20-m 
wide river between them. 

Local population density varied from 13.7 to 70.7 adults 
collected in 3 min or from 0.7 to 17.7 individuals collected 
per m* in 3 min (Table 1). However, the proportion of 
aphallic snails within a population was not correlated with 
local population density (number of snails collected in 3 
min: 7 = 0.17, n = 21, P = 0.47; number of snails/m? and 
3 min: r = 0.29, n = 21, P = 0.20). Furthermore, the 
proportion of aphallic snails was not correlated with the 
altitude of the locality (x = —0.24, n = 21, P = 0.29). 
Populations of Chondrina avenacea inhabit E-, S-, and 
W-exposed rock faces (Table 1). The exposure of the 
habitat had no significant effect on the proportion of aphal- 
lic individuals (one-way ANOVA, F = 0.66, df = 5, P= 
0.66). The number of other snail species co-occurring with 
C. avenacea ranged from 0 to 5 (Table 1), but had no 
significant effect on the proportion of aphallic individuals 
in C. avenacea (one-way ANOVA, F = 1.84, df = 5, P= 
0.17). Furthermore, the presence/absence of Clausilia par- 
vula and Pyramidula rupestris (which occurred at 16 [76.2%] 
and 12 [57.1%] of the 21 localities examined) had no effect 
on the proportion of aphallic individuals in Chondrina 
avenacea (presence/absence of Clausilia parvula: t = 0.89, 
df = 19, P = 0.38; P. rupestris: t = 0.12, df = 19, P= 
0.91). 

The populations varied significantly in adult shell size 
(Table 1). In general, aphallic snails were slightly smaller 
than euphallic ones (two-way ANOVA: population effect, 
F = 46.92, df = 20, P < 0.0001; sex type, F = 4.57, df = 
1, P = 0.033; interaction, = 1.65, df = 20, P = 0.034). 
The difference in shell height averaged 0.06 mm, which 
corresponds to 0.95% of the mean shell height or approx- 
imately to 2% of the total wet weight. Considering single 
populations, this difference was significant in only three 
of 21 populations (population 10: t = 3.76, n = 108, P < 
0.001; population 14: ¢ = 2.71, n = 90, P < 0.01; population 
21: t = 4.05, n = 251, P < 0.001). 

Mean shell size of Chondrina avenacea tended to decrease 
with local population density (r = —0.38, n = 21, P = 
0.09), which may indicate intraspecific competition. In 
contrast, mean shell size of C. avenacea was positively 
correlated with the number of other snail species present 
on the rock faces (Spearman rank correlation 7; = 0.65, n 
= 21, P= 0.0014), suggesting that some localities are more 
suitable for snails than other localities. Mean shell size 
was neither correlated with the altitude of the locality (r 
= 0.19, n = 21, P = 0.42) nor affected by the exposure of 
the rock face (one-way ANOVA, F = 2.17, df = 5, P= 
0.11). 


Allocation to Reproductive Structures 


Aphallic individuals from population 21 were signifi- 
cantly smaller (shell height) and slightly lighter (soft body 


B. Baur & X. Chen, 1993 


Page 255 


Table 1 


Percentage of alphallic individuals in natural populations of Chondrina avenacea in the surroundings of Basel (northwestern 
Switzerland), with local population density, shell size of fully grown snails, and habitat characteristics. 


Population 
% aphallic density? 
Locality? snails n x + SE 

1 14.0 114 54.7 + 5.6 
2 0.9 109 43.0 + 2.7 
3 6.4 110 Sl0) 25 Zei/ 
4 89.2 74 18.0 + 2.5 
5 6.2 112 30I3E 3i4 
6 1165) 65 Wed as) 1168) 
7 21.3 108 6 V7.0) 5 (O58) 
8 67.6 102 BAe eZ. 
9 77.4 84 les) ae Seo) 
10 76.9 108 S8o1/ 25 OY) 
11 14.9 101 33.3 + 2.4 
12 14.4 104 (oss) 23 2h) 
13 19.8 91 SOOM 229 
14 84.8 92 20.0 + 3.0 
15 78.4 116 49.3 + 3.9 
16 70.3 118 70.7 + 4.1 
17 43.1 102 1Q)35) 25) Aes) 
18 8.2 85 NS se SIA! 
19 Soo) ay 49.0 + 2.1 
20 64.1 103 46.7 + 3.2 
21 49.5 273 Sei as 2) 


Shell height (mm) Altitude 
KE SE (m) Exposure Other species‘ 
5.98 + 0.03 720 S 0) 
6.37 + 0.03 550 SW 1 
6.29 + 0.03 600 S) 1 
6.25 + 0.03 400 E 1 
6.41 + 0.03 410 SW 5 
6.80 + 0.05 590 NE 5 
6.56 + 0.03 500 Ww 2 
6.20 + 0.03 590 WwW 1 
6.43 + 0.04 440 SW 3 
6.42 + 0.03 610 E 2 
5.87 + 0.03 500 S 1 
7.06 + 0.03 580 W 3 
6.49 + 0.04 460 S 2 
6.39 + 0.04 440 SW 2 
6.17 + 0.03 610 Ss 2 
6.45 + 0.03 510 Ww 2 
6.74 + 0.03 720 SW 1 
6.88 + 0.04 650 E 4 
6.71 + 0.03 630 SE 3 
6.26 + 0.03 510 S 2 
6.45 + 0.02 490 W 2 


* For location of sites see Figure 1. 
* Number of fully grown snails collected within 3 min. 


‘ Other species included: family Cyclophoridae: Cochlostoma septemspirale (Razoumowsky); family Pyramidulidae: Pyramidula rupestris 
(Draparnaud); family Orculidae: Orcula dolium (Draparnaud); family Chondrinidae: Abida secale (Draparnaud); family Enidae: Ena 
montana (Draparnaud); family Clausiliidae: Cochlodina laminata (Montagu), Clausilia parvula Ferussac, Macrogastra plicatula (Dra- 
parnaud), Lacinaria plicata (Draparnaud); family Helicidae: Helicigona lapicida (Linneé). 


dry weight) than euphallic snails (Table 2). However, 
differences in soft body mass disappeared after differences 
in shell were controlled for (t = 0.33, df = 22, P = 0.74). 
Irrespective of size, individuals of both sex types differed 
in allocation to reproductive structures, which averaged 
28.3% of the total body mass in aphallic snails and 31.7% 
in euphallic snails (Table 2). The male copulatory organs 
of euphallic snails amounted to 3.2% of the total soft body 
weight (or to 9.9% of the reproductive structures), which 
corresponds approximately to the difference in allocation 
to reproductive structure measured between the two sex 
types (3.4%; Table 2). 


Seasonal Changes in Weight of 
Reproductive Structures 


Figure 2 shows the percentage of aphallic individuals 
collected from population 21 at monthly intervals between 
April 1991 and March 1992. The frequency of aphallic 
snails did not change significantly in the course of one year 
(x? = 10.67, df = 11, P > 0.4). This indicates that indi- 
viduals of Chondrina avenacea did not change their sex 
type. 

Figure 3 shows the seasonal variation in the relative 
weight of the reproductive structures for aphallic and eu- 


phallic Chondrina avenacea. The reproductive structures of 
euphallic snails were throughout the year heavier than 
those of aphallic snails. 


DISCUSSION 
Variation in Aphally Among Populations 


Our study demonstrated a large variation among pop- 
ulations in the percentage of aphallic individuals. The 
range of variation (0.9-89.2%) exceeds that found in nat- 
ural populations of Chondrina clienta on the Baltic island 
of Oland, Sweden (52.2-99.1%; BAUR et al., 1993). Com- 
paring both studies, aphallic individuals appear to occur 
more frequently in C. clienta (grand mean: 77.7%) than 
in C. avenacea (grand mean: 41.2%). This suggests that C. 
avenacea might on average have a higher outcrossing rate 
than C. clienta. 

The degree of allozyme variation is often considered as 
an indicator of the type of breeding system employed (e.g., 
SELANDER & OCHMAN, 1983; BROWN & RICHARDSON, 
1988). Enzyme electrophoresis revealed that all individuals 
in the samples from five populations of Chondrina clienta 
on Oland were homozygous and allelically identical at each 
of the 17 putative loci assayed (BAUR & KLEMM, 1989). 


Page 256 


The Veliger, Vol. 36, No. 3 


Table 2 


Shell height and dry weight of soft body and reproductive structures of aphallic and euphallic Chondrina avenacea 
from population 21. Mean values based on 12 monthly samples are presented. 


Aphallic snails 


Variable (@ = SE) 
Shell height (mm) 6.38 + 0.02 
Soft body dry weight (mg) 1.411 + 0.037 
Reproductive organs 
dry weight (mg) 0.401 + 0.018 
% soft body 28.3 + 0.8 


Male copulatory organs 
dry weight (mg) — 
% soft body — 


The lack of heterozygosity in C. clienta suggests that self- 
fertilization is the prevailing breeding system. Correspond- 
ing data are not available for C. avenacea. 

As in Chondrina clienta, the variation in genital dimor- 
phism in populations of C. avenacea did not follow any 
discernible geographic pattern, nor was it associated with 
any particular habitat characteristic. Genital dimorphism 
in C. avenacea might be adapted to fine-grained, so far 
unknown ecological conditions of the snails’ habitat. We 
found no intermediate stage in which the penis was only 
partly developed; it was always either present or absent. 
In population 21, the proportion of aphallic C. avenacea 
remained constant in monthly samples over one year. Sim- 
ilarly, POKRYSZKO (1987) found no seasonal changes in 
the percentage of aphallic individuals in a population of 
Vertigo pusilla Miller in Poland. All evidence so far avail- 
able indicates that individuals become either euphallic or 
aphallic during ontogeny and that, later at the adult stage, 
they are unable to resorb or build up male copulatory 
organs (LARAMBERGUE, 1939; POKRYSZKO, 1987, 1990; 
BAvuR et al., 1993). 

We found no correlation between the proportion of 
aphallic snails and local population density. This suggests 
that the frequency of aphally is not a simple function of 


100 


n 
Ee 
3 80 
ee 
- 60 
A) = 
Y 
a. gan? 
= 207 7 
0 AIST AS HORNED SEEN 
1991 1992 


Figure 2 


Seasonal variation in percentage of aphallic Chondrina avenacea 
collected at monthly intervals from population 21. 


Euphallic snails 


(x + SE) t-value P 
6.53 + 0.03 4.59 <0.001 
1.496 + 0.038 1.58 0.127 
0.476 + 0.025 2.41 0.025 
Shey Sele 2.38 0.026 
0.047 + 0.003 — — 

BO) ia (OH) — —— 


the mate encounter rate. Breeding experiments revealed 
that both genetic and nongenetic components may influence 
the proportion of aphallic offspring in the freshwater snail 
Bulinus truncatus (LARAMBERGUE, 1939; SCHRAG et al., 
1992). SCHRAG & READ (1992) found that the temperature 
experienced during the egg and hatching stage affected 
phally determination in two populations of B. truncatus. 
Little is known concerning the determination of genital 
dimorphism in land snails. POKRYSZKO (1990) reported 
that one euphallic and two aphallic individuals of Vertigo 
pusilla did not differ in the proportion of aphallic and 
euphallic offspring produced by selfing. BAUR et al. (1993) 
raised juveniles of Chondrina clienta in the laboratory to 
examine whether different conditions of food supply and 
population density experienced during ontogeny affect the 
expression of genital dimorphism. Snails from one popu- 
lation become euphallic more frequently under conditions 
of low food supply than expected under complete genetic 
determination. This suggests that, in addition to a genetic 


50 
40 
30 
20 


10 


% soft body mass 


AM J J AS O N DoJ Rem 
1991 1992 
Figure 3 


Seasonal variation in dry weight of reproductive structures of (Q) 
aphallic and (M) euphallic Chondrina avenacea collected at month- 
ly intervals from population 21. 


B. Baur & X. Chen, 1993 


component, the expression of the genital dimorphism can 
be influenced by environmental conditions. However, de- 
tailed breeding experiments are needed to elucidate the 
mechanism of the determination of genital dimorphism in 
land snails. 

Mean shell size of Chondrina avenacea tended to decrease 
with local population density, indicating intraspecific com- 
petition. Similarly, shell size of C. clienta was negatively 
correlated with local population density on the Baltic island 
of Oland (BAUR, 1988). Experiments demonstrated that 
intraspecific competition affects juvenile growth rate, age 
at maturity, adult shell size, and survival of C. clienta 
(BAUR & Baur, 1990). The observed competitive inter- 
actions appeared to be a result of both exploitation and 
interference by mucus trails (BAUR & BAurR, 1990). 


Allocation to Reproductive Structures 


Simultaneous hermaphroditism is assumed to be advan- 
tageous in animals of low mobility and in animals that 
live in low-density populations, for it decreases the risks 
of fitness loss as a result of lack of mating partners 
(TOMLINSON, 1966; GHISELIN, 1969; CHARNOV, 1982). 
Hermaphroditism also offers opportunities for self-fertil- 
ization. However, hermaphroditism carries increased fixed 
costs because each parent must build and maintain two 
sets of reproductive apparatus. A hermaphrodite therefore 
has less resources to invest in gametes and would be ex- 
pected to produce fewer eggs and sperm than gonochoristic 
equivalents (HEATH, 1977). The fixed costs of hermaph- 
roditism can be reduced by organ sharing in the repro- 
ductive system (HEATH, 1977). For example, the gonad 
(hermaphroditic gland) of pulmonate snails has a shared 
structure for producing both eggs and sperm. Aphally may 
be another way to reduce fixed costs for hermaphroditic 
snails with frequent or obligate selfing. Due to the reduced 
fixed costs for the reproductive structures, aphallic snails 
might have more energy for growth and reproduction 
(JARNE & DELAy, 1991). Indeed, aphallic individuals of 
Bulinus truncatus (a species with indeterminate growth) 
were larger and produced more eggs than euphallic snails 
of the same age (JARNE et a/., 1992). In contrast, our results 
indicate that aphallic Chondrina avenacea were smaller and 
invested less energy into reproductive structures than eu- 
phallic individuals. In C. clienta, the male reproductive 
structures develop during the subadult stage; the sex type 
could be assessed in individuals larger than 4.7 mm (BAUR 
et al., 1993). However, the genitals were not fully devel- 
oped before shell growth had been completed. Thus, the 
sex type appears to be determined before the final adult 
size is attained. Nonetheless, aphallic individuals of C. 
avenacea may invest less resources in growth and repro- 
ductive structures than euphallic ones. Consequently, one 
would expect that aphallic snails have an enhanced re- 
productive output. Experiments are needed to test this 
hypothesis. 

The present study demonstrated a great variation in the 


Page 257 


proportion of aphallic individuals in natural populations 
of Chondrina avenacea. This indicates that the rates of 
outcrossing and self-fertilization may vary among popu- 
lations. However, the selective forces that shape the pre- 
vailing mating patterns are still unknown. 


ACKNOWLEDGMENTS 


We thank A. Baur for help collecting snails. A. Baur, G. 
Bernasconi, and S. C. Stearns commented on the manu- 
script. Financial support was provided by the Swiss Na- 
tional Science Foundation (grant 31-33511.92 to BB). 


LITERATURE CITED 


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on winter survival of the rock-dwelling land snails Chondrina 
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Baur, A., B. BAUR & L. FROBERG. 1992. The effect of lichen 
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Baur, B. 1988. Microgeographical variation in shell size of 
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Baur, B. & A. BAuR. 1990. Experimental evidence for intra- 
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Baur, B., X. CHEN & A. BAUR. 1993. Genital dimorphism in 
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the influence of the environment on its expression. Journal 
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Baur, B. & M. KLEMM. 1989. Absence of isozyme variation 
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BREvURE, A. S. H. & E. GITTENBERGER. 1982. The rock-scrap- 
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Brown, K. M. & T. M. RICHARDSON. 1988. Genetic poly- 
morphism in gastropods: a comparison of methods and hab- 
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CuHarnov, E. L. 1982. The Theory of Sex Allocation. Princeton 
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GHISELIN, M. T. 1969. The evolution of hermaphroditism 
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208. 

GITTENBERGER, E. 1973. Beitrage zur Kenntnis der Pupillacea 
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Gouyon, P. H. & D. Couver. 1987. A conflict between two 
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JARNE, P. & B. DELAY. 1991. Population genetics of freshwater 
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JARNE, P., L. Finot, C. BELLEC & B. DELay. 1992. Aphally 


Page 258 


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The Veliger 36(3):259-264 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A New Species of Otostoma (Gastropoda: Neritidae) 


from Near the Cretaceous/Tertiary Boundary at 


Dip Creek, Lake Nacimiento, California 


RICHARD L. SQUIRES 


Department of Geological Sciences, California State University, 
Northridge, California 91330, USA 


LOUELLA R. SAUL 


Invertebrate Paleontology Section, Natural History Museum of Los Angeles County, 
900 Exposition Boulevard, Los Angeles, California 90007, USA 


Abstract. A neritid gastropod Otostoma aethes Squires & Saul, sp. nov., from uppermost Cretaceous 
or possibly lowermost Paleocene strata on the south side of Lake Nacimiento, San Luis Obispo County, 
California, is the only confirmed occurrence of this genus from the Pacific coast of North America. The 
presence of this Tethyan genus is suggestive of a warm K/T boundary climate. 


INTRODUCTION 


A new species of a large-sized neritid gastropod is described 
from a locality in marine strata in the Dip Creek area, 
northern San Luis Obispo County, central California (Fig- 
ure 1). The strata are important because they were de- 
posited near the Cretaceous-Tertiary boundary and per- 
haps include the boundary. Gastropods, as well as bivalves, 
of this age are poorly known on the Pacific coast of North 
America, and more than half of the species remain un- 
described (SAUL, 1986). 

The Dip Creek fauna contains some mollusks that re- 
semble genera or species usually considered to indicate a 
Paleocene age, as well as some indicative of a Cretaceous 
age. TALIAFERRO (1944) did not construe the mixture of 
ages to indicate closeness to the Cretaceous-Tertiary 
boundary but apparently interpreted the mixture as a re- 
sult of redepositon of Cretaceous rocks within Paleocene 
sediments. Within these sediments, however, there is not 
a segregation of “Cretaceous forms” from ‘Paleocene 
forms” (SAUL, 1986). In the Dip Creek area, turritellas 
dominate the fauna. MERRIAM (1941) named and de- 
scribed the most common species as Turritella pachecoensis 
adelaidana, and TALIAFERRO (1944) assigned a Paleocene 


age to the enclosing rocks. SAUL (1983) restudied the tur- 
ritellas and assigned the Dip Creek species to 7. penin- 
sularis adelaidana Merriam, 1941, and 7. webb: Saul, 1983. 
She inferred a latest Maastrichtian and possibly an earliest 
Paleocene age for the strata there. 

At Dip Creek, the turritellas and other mollusks are 
shallow-water forms that have undergone post-mortem 
transport and are within deep-water turbidites in beds of 
coarse-grained grit or conglomerate (GROVE, 1986). TAL- 
IAFERRO (1944) referred the Dip Creek strata to his Dip 
Creek Formation, but he was not aware of the sedimen- 
tologic and stratigraphic complexities in the area. DURHAM 
(1968) mapped the outcrops along the north shore of Lake 
Nacimiento as unnamed Upper Cretaceous and lower Ter- 
tiary rocks, and GROVE (1986) used this designation for 
the outcrops along the south shore of the lake. Confident 
assignment of the Dip Creek section to a formation can 
be done only after much-needed detailed geologic mapping 
in the Lake Nacimiento/Dip Creek area is undertaken 
(V. M. Seiders, personal communication). 

TALIAFERRO (1944:516) listed only 12 taxa from the 
Dip Creek Formation, and at least three of these [Amau- 
rellina sp., Tornatellaea pinguis (Gabb, 1864), and Turri- 
tella infragranulata Gabb, 1864] were undoubtedly from 


Page 260 


Figure 1 


Location map for UCMP loc. B-2368, Lake Nacimiento area, 
San Luis Obispo County, California. (After SAUL, 1986:fig. 1). 


outcrops northwest of Chimney Rock along Godfrey Road. 
These rocks were excluded from Taliaferro’s Dip Creek 
Formation and Durham’s unnamed Upper Cretaceous and 
lower Tertiary rocks by HOWELL et al. (1977), who rec- 
ognized them as a flysch sequence conformably overlying 
the unnamed Upper Cretaceous and Tertiary rocks, but 
with a probable hiatus between. DURHAM (1968) provided 
a list of mollusks from near the base of this flysch sequence 
indicative of a late early Paleocene age (about zone P3) 
(SAUL, 1983, 1986). Of the remaining nine taxa listed by 
TALIAFERRO (1944), the three purported 7urritella species 
are all 7. peninsularis adelaidana, and this subspecies is by 
far the most abundant taxon present. The only other spe- 
cies that can be considered to be of common occurrence is 
Venericardia (Pacificor) taliaferror. Verastegui, 1953. Nei- 
ther Calva (Calva) baptisia Saul & Popenoe, 1992, nor 
Turritella webbi Saul, 1983, is common. SAUL (1986) listed 
or figured 10 or more undescribed species, and most of 
these are represented by one or two specimens. If the 
composition of this fauna from very near the K/'T bound- 
ary is to be recorded, the descriptions will apparently have 
to be based, in most cases, on very few specimens. 

A single specimen of Otostoma aethes sp. nov. was found 
by N. L. Taliaferro in 1943(?) at University of California 
Museum of Paleontology (Berkeley) [= UCMP] loc. 
B-2368, along the south shore of Lake Nacimiento, at the 
east side of Dip Creek near the base of a canyon wall, 
120°55'40’N, 35°43’45"W, NE % NE % of section 30, 


The Veliger; Vola365Nom8 


T25S, R10E, U.S. Geological Survey, 7.5-minute, Lime 
Mountain, California, quadrangle, 1948 (photorevised 
1979), San Luis Obispo County, central California. The 
specimen was enclosed in hard, coarse-grained sandstone 
that required considerable effort by the junior author to 
remove. 

The outcrops in Dip Creek are usually covered by wa- 
ters behind the Lake Nacimiento dam but are exposed 
during drought years. In 1977, 1985, and 1986, the junior 
author visited the vicinity of UCMP loc. B-2368 but was 
unable to find any more specimens of the new species. We 
are reluctant to name a new species based on a single 
specimen, but the likelihood of finding more specimens is 
remote. 


SYSTEMATIC PALEONTOLOGY 
Family NERITIDAE Rafinesque, 1815 
Subfamily NERITINAE Rafinesque, 1815 
Genus Otostoma d’Archiac, 1859 


Desmieria DOUVILLE, 1904:344-346. COSSMANN, 1925:199- 
203. 


Type species: Nerita rugosa Hoeninghaus, 1830, non 
Gmelin, 1791; = Natica rugosa Goldfuss, 1844, non Bosc, 
1801; = Natica subrugosa d’Orbigny, 1850 (new name) [= 
Nerita rugosa Roemer, 1841; ? = Otostoma ponticum d’Ar- 
chiac, 1859], by indication DOUVILLE (1904:346). 


Discussion: Otostoma has a globose shell, with a low spire, 
rapidly expanding whorls, and collabral ornamentation. 
Some species have some subordinate spiral sculpture, es- 
pecially about the base, that tends to be broken into nodes 
by the collabral ribs. The deck is broad and reduces the 
apertural opening. The inner lip has several large teeth 
that extend onto the roundly callused deck. The collabral 
sculpture and roundly callused deck readily distinguish 
typical Otostoma from Nerita Linné, 1758. 

D’ARCHIAC (1859) listed five species in his new genus: 
Otostoma tchihatcheffi d@ Archiac, O. ponticum d’Archiac, O. 
rugosum dArchiac, O. pouechi d’Archiac, and O. valen- 
ciennest d’Archiac, but chose no type species. Although all 
are listed as though d’Archiac were the author, for O. 
rugosum d’Archiac, he provided a synonomy consisting of 
“Natica rugosa, Hoeninghaus, Goldfuss, p. 119, pl. 199, 
fig. 11a, b (a poor picture), N. subrugosa, d’Orbigny, Pro- 
drome, p. 221.” Additionally he mentioned that some of 
the specimens examined by him are from the upper part 
of the ‘‘craie de Maastricht.”’ He excluded, because the 
figure is too poor, Nerita rugosa ROEMER (1841:83, no. 1, 
pl. 12, fig. 6), which D’OrRBIGNy (1850) had included in 
his replacement name Natica subrugosa. 

DOUVILLE (1904) proposed the name Desmieria as a 
replacement name for Otostoma d’Archiac because of the 
supposed conflict with Otostomus Beck, 1837, and desig- 
nated as type of Desmieria the best known species “Desm. 


R. L. Squires & L. R. Saul, 1993 


rugosa, de la craie de Maastrict,’ Netherlands. The type 
species of Desmieria is therefore, by original designation, 
one of the species d’Archiac included in Otostoma. Douvillé 
thus set the type species of Otostoma by indication because 
fixing the type species of either the original or the replace- 
ment name fixes the type species of the other (RIDE et al., 
1985, article 67). That Douvillé referred to the type species 
only as Desmieria rugosa does not prevent its recognition 
as the Otostoma rugosum listed by d’Archiac, because both 
Douvillé and d’Archiac referred to its occurrence in the 
craie de Maastricht. KEEN & Cox (1960) indicated that 
Natica rugosa Roemer, 1841, is the type species by sub- 
sequent designation of COSSMANN (1925:199), although 
Cossmann actually presented Nerita rugosa Hoeningh. as 
the type species of Desmieria, probably following Douvillé’s 
indication, which is earlier and adequate. 

Several authors, including DARTEVELLE & BREBION 
(1956), GLIBERT (1962), and WENZ (1938), have listed 
the type species of Otostoma as O. ponticum d’Archiac. The 
source of this may be FISCHER (1887:800), who listed O. 
ponticum d’Archiac in parentheses. Although FISCHER 
(1880-1887) in many cases explicitly indicated type species 
in parentheses, he also did the same for examples. In the 
case of Otostoma he failed to indicate whether O. ponticum 
should be considered the type species or only an example, 
and he cannot be considered to have designated the type. 

The first usage that we have found of the specific name 
rugosa for the Otostoma from the “‘craie de Maastricht”’ is 
that of HOENINGHAUS (1830:467) in the combination Neri- 
ta rugosa. Natica rugosa has also been used (ROEMER, 1841; 
HOENINGHAUS in GOLDFuss, 1844). Both combinations 
are junior primary homonyms; for the former, Nerita ru- 
gosa Gmelin, 1791, has priority and for the latter, Natica 
rugosa Bosc, 1801, for both of which D’OrRBIGNY (1850) 
provided Natica subrugosa d’Orbigny, 1850. 

DOUVILLE (1904) also recognized that there are three 
different groups among D’ARCHIAC’s (1859) five species 
of Otostoma. The first three, O. tchihatcheffi, O. ponticum, 
and O. rugosum, and Otostoma; O. pouechi is a Corsania; 
and O. valenciennesi may be a Velates Montfort, 1810. 


Otostoma aethes Squires & Saul, sp. nov. 
(Figures 2-4) 


Diagnosis: An Otostoma with prominent shoulder on body 
whorl, a few low spiral ribs on anterior third of body 
whorl, noded at intersections by low collabral ribs; deck 
broad and rather flat with seven subequal teeth along inner 
lip margin. 


Description: Shell thick, medium sized, height 30 mm, 
width 27.3 mm. Body whorl rapidly expanding with sub- 
angulate shoulder. Spire very low, apex elevated slightly 
above flattened dorsal surface. Sculpture of several low 
collabral swellings, most prominent adaperturally, strong- 
ly prosocline, and fairly prominent on dorsal area near 
outer lip; anterior third of body whorl with three very low 


Page 261 


spiral ribs, faintly noded at intersection with collabral 
swellings; posteriormost spiral obsolete adaperturally. 

Aperture large, somewhat quadrate, anterior end trough- 
shaped. Outer lip sturdy, beveled anteriorly. Deck broad, 
much reducing aperture, with seven teeth along slightly 
curved inner lip margin; anteriormost two teeth small, next 
two strongest, next two moderately strong, and posterior- 
most one small. Four strongest teeth extend onto deck as 
elongate, flat projections with intervening deep pits. Deck 
area flattened with thin callus. Numerous minute and 
closely spaced growth lines on body whorl. 


Holotype: UCMP 398607. 


Type locality; UCMP loc. B-2368, Dip Creek, at the 
narrows, south shore of Lake Nacimiento, San Luis Obispo 
County, central California, 120°55’40"N, 35°43'45”"W. 


Discussion: The specimen has been damaged. The abrupt 
change in coiling of the body whorl is attributable to post- 
burial compression. The deck has been broken off from 
its juncture with the anterior part of the aperture and 
pushed into the aperture. The entire deck has been dis- 
placed approximately 2 mm posteriorly. The deep pits 
surrounding the extensions of the four strongest teeth onto 
the deck are probably the result of absorption of shell 
material by the animal or post-mortum dissolution of the 
deck area. Neritids are known to resorb internal shell 
structures (WOODWARD, 1892; COSSMANN, 1925) and pro- 
duce shells that are subject to differential dissolution. The 
neritid shell has an external layer of calcite and one or 
more inner layers of aragonite (BOGGILD, 1930; WILBUR, 
1964). The inner lip callus is especially prone to post- 
mortum dissolution, and the genus Otostoma was originally 
characterized as lacking a neritid inner lip and columella 
(D’ARCHIAC, 1859) because the available specimens had 
undergone selective dissolution (BINKHORST, 1861). 

The new species is most similar to Otostoma divaricata 
(D’ORBIGNY, 1847:pl. 4, figs. 43, 44), an apparently widely 
distributed species that has been reported from both the 
Upper Cretaceous of southern India (STOLICZKA, 1868: 
340-341, pl. 23, figs. 11, 12; pl. 28, fig. 5) and Hungary 
(PETHO, 1906:127-130, pl. 9, figs. 11-17). KEEN & Cox 
(1960:fig. 183, figs. 14, 14a) figured O. divaricata from the 
Upper Cretaceous of Hungary as the illustration for the 
genus Otostoma. STOLICZKA (1868) reported the latter spe- 
cies from the southern India “‘Arrialoor” Group, which is 
of Campanian to Maastrichtian age according to SASTRY 
et al. (1968). The age of O. divaricata in Hungary is Maas- 
trichtian according to COSSMANN (1925:203). PETHO’s il- 
lustrations of O. divaricata show that there is considerable 
variation in this species. Some of his specimens are similar 
to O. aethes in size and in having the following morpho- 
logic features: spiral ribs in the anterior third of the body 
whorl, collabral ribs much stronger than the spiral ribs, 
strong teeth on the inner lip, and an angulate shoulder on 
the body whorl. Otostoma aethes differs in having a larger 
dorsal surface, narrower and more elongate aperture, an 


Page 262 


The Veliger, Vol. 36, No. 3 


Explanation of Figures 2 to 4 


Figures 2-4. Otostoma aethes Squires & Saul, sp. nov., holotype, UCMP 398607 from UCMP loc. B-2368, x 1.6. 
Figure 2. Apertural view. Figure 3. Abapertural view, low-level lighting used to show subdued sculpture. Figure 


4. Dorsal view. 


inner lip callus apparently nearly flat, subequal teeth on 
the inner lip, and in being less globose with a shorter spire 
and a more angulate shoulder. 

The flattened inner lip area renders Otostoma aethes an 
atypical Otostoma, but its collabral sculpture and the pat- 
tern of the teeth on the inner lip are not found in Nervta. 

WENz (1938) and Davies (1971) reported the geologic 
range of Otostoma to be Cretaceous to Paleocene and its 
distribution to be cosmopolitan. GLIBERT (1962), however, 
reported O. equinus (Bezancgon, 1870) from the middle 
Eocene (Lutetian) of the Paris Basin, France. Most work- 
ers have assigned equinus to Velates Montfort, 1810, which 
is closely allied with Otostoma. Woops & SAUL (1986) also 
believed that equinus and probably Velates noorpoorensis 
(d’Archiac & Haime, 1854) of the Eocene of India should 
be placed in Otostoma. Velates batequensis Squires & De- 
metrion, 1990, from the lower Eocene of Baja California 
Sur, Mexico, is also very closely allied to Equinus. Juvenile 
specimens of equinus have characteristics of Otostoma 
whereas adult specimens have characteristics of Velates. 
More work is needed to fully resolve the taxonomic position 
of these ribbed neritids. 

Otostoma is a Tethyan genus and most species are from 
the Old World Tethyan paleobiogeographic province. Pre- 
viously, the only report of Otostoma from the Pacific coast 
of North America was that of ALLISON (1955:414, pl. 40, 
figs. 11, 12), who reported specimens of the Japanese 
species Otostoma japonicum (Nagao, 1934) from the Mid- 
dle Cretaceous (upper Aptian, Alisitos Formation) of Baja 
California, Mexico. Allison’s figured specimen has a con- 
cave ramp area and a noded shoulder; it is smaller, has a 
more elevated spire, and has stronger collabral ribs on the 
spire than O. aethes. As mentioned by Woops & SAUL 
(1986), neither Allison’s figured specimen nor “‘Otostoma”’ 
japonicum (Nagao) belong to Otostoma; both belong instead 
to the genus Corsania Vidal, 1917. The Alisitos Formation 


material differs enough from Corsania japonicum to con- 
stitute a new species. Desmieria peruviana Olsson, 1934, 
from the Late Cretaceous of the Amotape region, Peru, is 
also a Corsania. The genus Otostoma is closely related to 
Corsania, but in Corsania the spiral sculpture is dominant, 
especially about the mid-whorl, the whorl is distinctly 
angulate rather than globular in profile, and the angula- 
tions are emphasized by strong nodes. DOUVILLE (1904) 
recognized these two groups but retained both within Des- 
mieria [= Otostoma]. A number of species of Corsania, in- 
cluding Allison’s species from the Alisitos Formation and 
Corsania japonica (Nagao) from Japan, will need to be 
reallocated before the geologic range and paleogeographic 
distribution of Otostoma can be more accurately under- 
stood. 

Additional species of Otostoma in the United States are 
O. apparata Cragin, 1893 [as Neritina], O. marcouana Cra- 
gin, 1895 [as Neritoma], and O. pecosensis Stanton, 1947 
{as Nerita?]. All are from Lower Cretaceous (Comanchian 
Series) of Texas and are discussed and illustrated in 
STANTON (1947). Unlike the new species, all are very small 
and have a fairly elevated spire and a more rounded shoul- 
der on the body whorl. 

Other nerites known from Cretaceous strata of the Pa- 
cific coast of North America are Nerita (Bajanerita) cali- 
forniensis (White, 1885) and Neritina (Dostia) cuneata 
(Gabb, 1864). The subgenus Bajanerita Squires, 1993, 
present in the Rosario Formation of early Maastrichtian 
age in Baja California, Mexico, is characterized by its 
small size, only three very wide but strong teeth on the 
inner lip, and many small teeth on the outer lip. Woops 
& SAUL (1986) suggested placing Nerita cuneata Gabb, 
1864, in Neritina (Dostia) rather than Velates, where STEW- 
ART (1927) had placed it. 

The only Paleocene nerite reported from the Pacific 
coast of North America is a possible new species of Nerita 


R. L. Squires & L. R. Saul, 1993 


Page 263 


(Theluostyla) said to be from the Sepultura Formation near 
Punta Rosario, Baja California, Mexico (Woops & SAUL, 
1986). It is much smaller than Otostoma aethes, has 18 
granulate spiral ribs on the body whorl, and has numerous 
teeth on the outer lip. As mentioned by SQuIREs (1992), 
Eocene strata of the Pacific coast of North America, of the 
Paris Basin, France, and of Hungary have also yielded 
various species of Nerita (Theliostyla). They share similar 
features that differentiate them from O. aethes. 

Otostoma aethes sp. nov. is the only neritid known from 
strata of latest Maastrichtian to earliest Paleocene age on 
the Pacific coast of North America. It is also the only 
Otostoma known from this region and may indicate a very 
late Maastrichtian Tethyan-influenced influx of warm- 
water conditions at the K/T boundary. 


Etymology: The name is derived from the aethes, Greek, 
meaning unusual or strange. 


Occurrence: Latest Maastrichtian or possibly earliest Pa- 
leocene, unnamed strata, Dip Creek, south shore of Lake 
Nacimiento, San Luis Obispo County, central California. 


ACKNOWLEDGMENTS 


David L. Lindberg (UCMP) loaned the specimen. Victor 
M. Seiders (U.S. Geological Survey, Menlo Park) shared 
his knowledge about the stratigraphy of the Dip Creek 
area and provided transport (by way of his boat) for the 
junior author to visit the Dip Creek area. Lindsey T. 
Groves (Natural History Museum of Los Angeles County, 
Malacology Section) and Richard B. Saul provided some 
key literature. George L. Kennedy and Edward C. Wilson 
(Natural History Museum of Los Angeles County, In- 
vertebrate Paleontology Section) critically read an early 
draft of the manuscript. Two anonymous referees are 
thanked for their helpful comments. 


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The Veliger 36(3):265-269 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


The Nautilid Eucymatoceras (Mollusca: Cephalopoda) 


in the Lower Cretaceous of Northern California 


by 


PETER U. RODDA, MICHAEL A. MURPHY, ano CLARENCE SCHUCHMAN 


California Academy of Sciences, San Francisco, California 94118, USA 


Abstract. 


Three specimens of the nautilid Eucymatoceras plicatum (Fitton, 1836), characterized by 


chevron-shaped ribs, were collected from Lower Cretaceous (Aptian) rocks in northern California. This 
is the first record of the genus in California, and the second record in the Western Hemisphere. Previous 
records are from the Lower Cretaceous (Barremian and Aptian) of western and southeastern Europe 


and Baja California, Mexico. 


INTRODUCTION 


Among the numerous Cretaceous fossils collected during 
our many years of field work in the Cottonwood District 
of northern California are three specimens of the distinctive 
nautilid cephalopod Eucymatoceras. Two specimens are in 
the geology collections of the California Academy of Sci- 
ences (CASG); the third is from the former collections of 
the University of California, Los Angeles (UCLA), now 
at the Department of Invertebrate Paleontology, Los An- 
geles County Museum of Natural History (LACMIP). 
The purpose of this paper is to describe these specimens 
and compare them with previously described specimens. 


SYSTEMATIC PALEONTOLOGY 
MOLLUSCA 
CEPHALOPODA 
Family CYMATOCERATIDAE Spath, 1927 
Genus Eucymatoceras Spath, 1927 


Type species: Nautilus plicatus Fitton, 1836; by original 
designation (SPATH, 1927). 


Diagnosis: Conch rounded, depressed; suture slightly sin- 
uous, siphuncle subcentral; prominent coarse ribs in a 
chevron pattern with the principal V’s pointing adapically 
on the venter and adorally on the flanks. 


Discussion: Three species of Eucymatoceras were recog- 
nized by KUMMEL (1956:433) and by SHIMANSKY (1960: 
243-244): E. plicatum (Fitton, 1836) [= E. requienianus 
(@Orbigny, 1840)], E. stschurowsku (Milashevich, 1877), 
and E. steven: (Karakasch, 1907). KUMMEL (1956:433) 
notes that these three species have similar shaped shells, 


but he doubts that conch form in Eucymatoceras can be 
considered as species diagnostic. He mentions no other 
distinguishing characteristics. From published descriptions 
and illustrations, E. stschurowsku and E. steveni appear to 
differ from £. plicatus in the character of the ribbing. In 
E. stschurowsku the ribs are not straight and uniform but 
are irregularly angled in zig-zag fashion across the flank 
(MILASHEVICH, 1877:pl. 1, fig. 11). Eucymatoceras steveni 
differs in having an additional short chevron on the venter 
with the V pointing adorally, forming five chevron angles 
in all compared to the two chevron angles on other spec- 
imens of this genus. These distinctions are summarized by 
SHIMANSKY (1960:243-244). 

Our specimens and published illustrations of Eucyma- 
toceras demonstrate considerable variation in ribbing pat- 
tern including small chevrons intercalated between the 
larger ones, reversed rib angulation at the apertural flank 
edge, irregular truncation of ribs (incomplete chevrons), 
chevron number, chevron angle, and position of the chevron 
on the flank. Chevron angles measured from published 
illustrations and from the California specimens vary from 
45 to 80° on the venter and 30 to 95° on the flanks (Table 
1). The position of the flank chevron varies from mid-flank 
to ventrolateral. 

The variability in rib character expression, and place- 
ment do not appear to define consistent species-level groups. 
The three taxa (Eucymatoceras fittoni, E. stschurowski, and 
E. steveni) are based on differences in ribbing that we 
interpret as variation in a single species. Published de- 
scriptions and available specimens do not uniquely resolve 
this taxonomic problem. 


Occurrence: The genus is reported from Barremian and 
Aptian strata in England (FITTON, 1836; KUMMEL, 1956), 
France (D’ORBIGNY, 1840; KILIAN & REBOUL, 1915), Spain 


Page 266 The Veliger, Vol. 36, No. 3 


P. U. Rodda et al., 1993 


Page 267 


Table 1 


Chevron angles (degrees) of specimens of Eucymatoceras. 
Measurements were made directly from CASG and LAC- 
MIP specimens; the remainder are from published illus- 


trations. 
Ventral 
Flank chevron chevron 
(degrees) (degrees) 
CASG 60847.01 30 45 
CASG 60847.02 56 29, 38 
LACMIP 12100 = 30 
FITTON, 1836 55-60 55-60 
D’ORBIGNY, 1840 88-95 59-60 
MILASHEVICH, 1877 95-100 — 
UHLIG, 1883 40-58 — 
KARAKASCH, 1907 70-90 80-90 
KUMMEL, 1956 65-76 75-80 
SHIMANSKY, 1960:pl. 5 64-71 — 
DIMITROVA, 1967 40 60 
CALZADA & VIADER, 1980 59 47 
SUNDBERG, 1984 — 28, 30 


(BATALLER, 1962; CALZADA & VIADER, 1980), Czecho- 
slovakia (UHLIG, 1883), Bulgaria (DIMITROVA, 1967), 
Crimea (MILASHEVICH, 1877; KARAKASCH, 1907), Cau- 
casus (SHIMANSKY, 1960), Mexico (SUNDBERG, 1984), and 
California (herein). 


Eucymatoceras Plicatum (Fitton, 1836) 
(Figures 1-8) 


Nautilus plicatus FITTON, 1836: 129, fig. 1; Uhlig, 1883:178, 
pl. 3. 

Nautilus requienianus D’ORBIGNY, 1840:72-74, pl. 10. 

Nautilus stschurowski MILASHEVICH, 1877:121-122, pl. 1, 
fig. 11. 

Nautilus stevent KARAKASCH, 1907:30, pl. 2, fig. 13, pl. 8, 
fig. 12. 

Eucymatoceras plicatus (Fitton): KUMMEL, 1956:432, text- 
fig. 27, pl. 21; DimiTrova, 1967:17, pl. 1, figs. 1, 1a; 
CALZADA & VIADER, 1980: 164, pl. 2, figs. 2a, b. 

Eucymatoceras plicatum Fitton: SHIMANSKY, 1960:243, pl. 5, 
figs. 2, 3a—b. 

Eucymatoceras stevent Karakasch: SHIMANSKY, 1960:243, pl. 
6, figs. 1a—b. 


20 me 


s 


Weaverville 
SHASTA COUNTY 


f 
Cottonwood 


COUNTY 4 


; 


5 TEHAMA CO 


, 


Figure 9 


Map showing area of the Ono quadrangle (1:25,000) (open rect- 
angle) and locations of the large scale maps of Figure 10. 


Eucymatoceras stschurowsku Milashevich: SHIMANSKY, 1960: 
244, pl. 8, figs. 2a—b. 
Eucymatoceras sp.: SUNDBERG, 1984:43-46, fig. 2. 


Description and diagnosis: As for genus. 


Description of northern California specimens: Speci- 
mens are crushed, distorted, and partly eroded fragments 
from 150 mm to 230 mm in maximum dimension. 

The best preserved specimen, CASG 60847.01 (Figures 
1-4), is part of outer whorl, mostly body chamber, max- 
imum dimension 230 mm; inner whorls crushed, exposed 
in erosional cross section; four partial suture lines are 
straight to slightly sinuous; siphuncle not visible; ribs about 
3.5 mm wide, generally broadly arcuate, flat-topped and 
steep-sided in cross section; interspaces about 2 mm wide; 
chevron angles on venter and on flank about 45° and 30°, 


Explanation of Figures 1 to 8 


Figures 1-4. Eucymatoceras plicatum (Fitton, 1836). CASG 
60847.01, maximum dimension 230 mm. Figure 1. Ventral view. 
Figure 2. Ventral view from adapical end. Figure 3. Lateral 
view. Figure 4. Ventral view from adoral end. 


Figure 5. Eucymatoceras plicatum (Fitton, 1836). CASG 60847.02, 
maximum diameter 207 mm. Lateral view. 


Figures 6, 7. Eucymatoceras plicatum (Fitton, 1836). Private col- 
lection, present status unknown, maximum diameter (estimated) 
250 mm. 


Figure 8. Eucymatoceras plicatum (Fitton, 1836). LACMIP 12100 
(from UCLA 2972 = LACMIP 22972), maximum dimension 
150 mm. Ventrolateral view. 


, (e) 
\ es 
Belemnite Ses 
Wy f 


oz SNK \ 
‘  CASG 60847 


LE 


LENA 


Figure 10 


Maps of collecting localities, California Academy of Sciences 
Geology 60847 and Los Angeles County Museum Invertebrate 
Paleontology 22972. Base map is the Ono 1:25,000-scale metric 
topographic map (1981), contour interval 10 m. 


respectively (measurement of chevron angles is illustrated 
in Figure 11). Most ribs extend singly from umbilical edge, 
some bifurcate on inner flank; umbilical and peripheral 
ribs irregularly truncate one another (incomplete chev- 
rons), a feature well-shown in published illustrations 
(UHLIG, 1883:pl. 3; KUMMEL, 1956:pl. 21) (see Figure 
11). 

A second specimen, CASG 60847.02 (Figure 5), is a 


The Veliger, Vol. 36, No. 3 


Figure 11 


Illustration of measurement of chevron angles of ribs on Eucy- 
matoceras; measurement taken at apex of angle. Chevron angle 
changes irregularly with growth and increases as ribs curve from 
apex. Figure of EF. plicatus from UHLIG (1883). 


nearly complete whorl, maximum diameter 207 mm, se- 
verely crushed laterally with chevron ribs showing on three 
shell fragments near the apertural end of the conch. Chev- 
ron angles on ventral shell fragments are 29 and 38°; angle 
on flank shell fragment is 56°. Suture not exposed. 

The smallest specimen, LACMIP 12100 (from UCLA 
locality 2972 = LACMIP 22972) (Figure 8), maximum 
dimension 150 mm, is crushed and eroded with partial 
cross section of inner whorls exposed on inner side. Chev- 
ron angle on one ventral shell fragment is 30°. 

A fourth, exceptionally well-preserved specimen (Fig- 
ures 6, 7), from the North Fork of Cottonwood Creek, 
Shasta County, was collected by a local resident and was 
photographed in 1951 by M. A. Murphy. The present 
location of this specimen is unknown. 


Remarks: The California specimens generally have small- 
er chevron angles than those measured from published 
illustrations (Table 1). 


Localities: The northern California specimens came from 
the Budden Canyon Formation, upper Chickabally Mem- 
ber (MuRPHY ef al., 1964), Cottonwood District, south- 
west Shasta County, California (Figures 9, 10). 

CASG Locality 60847: Creek-bed exposure on the north 
side of the North Fork of Cottonwood Creek, 5 m upstream 
from the mouth of Belemnite Gulch, a small north-heading 
tributary (Figure 10). Two specimens (Figures 1-5). C. 
Schuchman and M. A. Murphy, collectors. 

LACMIP Locality No. 22972 [= UCLA 2972]: Ex- 
posure in south-heading tributary to Roaring River, ap- 
proximately 2 mile (1 km) east of Bland Road (Figure 
10; Murpny, 1956:fig. 4). One specimen. M. A. Murphy, 
collector. 


P. U. Rodda et al., 1993 


Age: All specimens are associated with or bracketed by 
fossils from the Gabbioceras wintunius zone, Upper Aptian 
(Gargasian) (MURPHY, 1956; MuRPHY et al., 1964). 


ACKNOWLEDGMENTS 


We thank several individuals and agencies for their help. 
Stephen Schuchman and George Shkurkin provided En- 
glish translations of Russian and Bulgarian publications. 
J. Latini and L. Westlake permitted physical access to the 
area. The National Science Foundation, U.S. Army Corps 
of Engineers, California Department of Water Resources, 
and University of California Riverside Intramural Re- 
search Fund provided financial support for the larger proj- 
ect of which this paper is a part. 


LITERATURE CITED 


BATALLER, J. R. 1962. Los cefalopodos del macizo Cretacico 
de Garraf (Barcelona). Barcelona Academia Ciencias y Artes, 
Memorias 34(8):174-211. 

CALZADA, S. & J. M. VIADER. 1980. Sobre dos nautilidos 
aptienses hallados en el nordeste Espanol. Estudios Geolo- 
gicos 36:163-167. 

Dimitrova, N. 1967. Les Fossiles de Bulgarie, IV, Crétacé 
inférieur, Cephalopoda (Nautiloidea et Ammonoidea). Aca- 
demie Bulgare des Sciences. 424 pp [in Bulgarian]. 

Fitton, W. H. 1836. Observations on some of the strata be- 
tween the Chalk and the Oxford Oolite, in the south-east of 
England. Geological Society of London, Transactions 2(4): 
103-388. 

KarRAKASCH, N. I. 1907. Le Crétacé inférieur de la Crimée et 


Page 269 


sa faune. Travaux de la Societe Imperiale des Naturalistes 
de St.-Petersbourg 32(5):1-482 [in Russian]. 

KILIAN, W. & P. REBOUL. 1915. Contribution a l’étude des 
faunes paléocrétacées du sud-est de la France. France, Ser- 
vice de la carte geologique, Memoires. 296 pp. 

KUMMEL, B. 1956. Post-Triassic nautiloid genera. Harvard 
College, Museum Comparative Zoology, Bulletin 114(7): 
1-494. 

MILASHEVICH, K. S. 1877. Paleontological sketches I, on some 
Cretaceous fossils from the Crimea. Moscow Imperial Na- 
ture Society, Bulletin 52:65-128 [in Russian]. 

Murpny, M. A. 1956. Lower Cretaceous stratigraphic units 
of northern California. American Association Petroleum Ge- 
ologists, Bulletin 40:2098-2119. 

Murphy, M.A., G. PETERSON & P.U. RoppA. 1964. Revision 
of Cretaceous lithostratigraphic nomenclature, northwest 
Sacramento Valley, California. American Association Pe- 
troleum Geologists, Bulletin 48:496-502. 

OrBIGNY, A. D’. 1840. Paléontologie Francaise, Terrains Cré- 
tacées, I. 662 pp. 

SHIMANSKY, V. N. 1960. Nautiloidea. Pp. 239-249. In: V. V. 
Druschits & M. P. Kudryavsteva (eds.), Atlas of Lower 
Cretaceous Fauna of the Northern Caucasus and Crimea. 
State Scientific-technical Publishers of Petroleum and Min- 
ing-fuel Literature: Moscow [in Russian]. 

SpaTH, L. F. 1927. Revision of the Jurassic cephalopod fauna 
of Kachh (Cutch). Geological Survey of India, Memoirs, 
Palaeontologica Indica, New Series 9(2):1-84. 

SUNDBERG, F. A. 1984. Two Cretaceous nautiloids from Baja 
California, Mexico and Southern California. Southern Cal- 
ifornia Academy of Sciences, Bulletin 83:43-52. 

UHLIG, V. 1883. Die Cephalopodenfauna der wernsdorfer 
Schichten. Wien, Akademie naturwissenschaft, Denkschrifte 
46:127-290. 


The Veliger 36(3):270-275 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Earliest Record of the Anomiid Bivalve 


Pododesmus: A New Species from the Lower 


Eocene of Western Washington 


RICHARD L. SQUIRES 


Department of Geological Sciences, California State University, 
Northridge, California 91330, USA 


Abstract. An anomiid bivalve, Pododesmus (Pododesmus) dunhamorum sp. nov., from lower Eocene 
shallow-marine strata in the upper part of the Crescent Formation on the west side of Dabob Bay, 
Jefferson County, eastern Olympic Peninsula, Washington, is the earliest known species of this genus 
and subgenus. The new species is one of two Eocene species of Pododesmus s.s. that inhabited hard 
substrate in nearshore waters along the Pacific coast of North America. The other species is P. (P.) 
inornatus (Gabb, 1864) from the middle Eocene of central California and southwestern Washington. 


INTRODUCTION 


Pododesmus sensu stricto (Bivalvia: Anomiidae) is known 
only from a few Tertiary fossil species in the Americas 
and New Zealand and two extant species in the Americas. 
The most widespread living species is Pododesmus (P.) rudis 
(Broderip, 1834), which is found byssally attached to rock, 
coral, shell, or other hard substrates in shallow waters 
along the coasts of South Carolina, Florida, Texas, Ber- 
muda, West Indies, Brazil, and central Argentina (CAR- 
CELLES, 1941; ABBOTT, 1974; Rios, 1975). According to 
ABBOTT (1974) and Rios (1975), Pododesmus leloirt Car- 
celles, 1941, from the Golfo San Matias, Argentina, is 
probably a synonym of P. (P.) rudis. The only other un- 
doubted living species of Pododesmus s.s. is P. (P.) foliatus 
(Broderip, 1834), which ranges from western Mexico to 
northern Peru (KEEN, 1971). 

Described herein is a new species of Pododesmus s.s. 
from lower Eocene strata in the upper part of the Crescent 
Formation, western Washington (Figure 1). This is the 
earliest record of this genus and subgenus. Previously, the 
earliest record of Pododesmus s.s. was from middle Eocene 
strata in central California and western Washington 
(WEAVER, 1942 [1943]). 

Abbreviations used for catalog and/or locality numbers 
are: CSUN, California State University, Northridge; 
LACM and LACMIP, Natural History Museum of Los 
Angeles County, Los Angeles, Malacology Section and 
Invertebrate Paleontology Section, respectively; UCMP, 
University of California Museum of Paleontology. 


STRATIGRAPHIC DISTRIBUTION 
AND GEOLOGIC AGE 


Pododesmus (P.) dunhamorum sp. nov. was found at three 
localities in the upper part of the Crescent Formation along 
the west side of Dabob Bay about 50 km west of Seattle, 
Jefferson County, Washington (Figure 1). Localities 
CSUN 1511 and 1512 are very near each other, and CSUN 
loc. 1502 is approximately 6 km farther north. Thirty- 
nine specimens were found, four at loc. 1502, 22 at loc. 
1511, and 13 at loc. 1512. All are single valves; four left 
valves, 12 right valves, and 23 of which the valve type 
cannot be determined. Preservation ranges from poor to 
good, and at loc. 1511, 40% of the specimens are molds. 

The lithologies at CSUN locs. 1511 and 1512 and their 
depositional environment and geologic age are discussed 
by SQUIRES et al. (1992). At both localities, there is fos- 
siliferous pebble conglomerate interbedded with basalt units 
that were extruded into very shallow-marine waters. Ero- 
sion of the basalts by storm waves produced rubble that 
was transported offshore, where substrate-attaching spe- 
cies, like Pododesmus (P.) dunhamorum, were able to 
inhabit it. The upper Crescent Formation in this area is 
late early Eocene in age on the basis of its contained cal- 
careous nannofossils, benthic foraminifera, and macrofos- 
sils. This age is equivalent to calcareous nannofossil Zones 
CP10-CP11, which straddle the boundary between the 
provincial molluscan “Capay Stage” and ‘“Domengine 
Stage.” 

Fossils from CSUN loc. 1502 were collected from boul- 


R. L. Squires, 1993 


der-sized blocks of Crescent Formation that are within a 
modern landslide. The strata at this locality are litholog- 
ically, macrofaunally, and paleoenvironmentally similar to 
those at CSUN locs. 1511 and 1512. The rocks in the two 
areas are coeval (SQUIRES, 1992). 


SYSTEMATIC PALEONTOLOGY 
Family ANOMIIDAE Rafinesque, 1815 
Genus Pododesmus Philippi, 1837 


Type species: Pododesmus decipiens Philippi, 1837 [= Pla- 
cunanomia rudis Broderip, 1834], by monotypy; Recent, 
South Carolina to Argentina. 


Subgenus Pododesmus s.s. 


Pododesmus (Pododesmus) dunhamorum 
Squires, sp. nov. 


(Figures 2-9) 


Anomiid (Pododesmus-like, new genus?): SQUIRES et al., 1992: 
7, table 1, pl. 1, figs. 28-29. 


Diagnosis: Medium-sized Pododesmus, ovate, sculpture of 
15 to 17 radial ribs on both valves; byssal foramen small, 
closed by a calcareous plug immediately adjacent to mod- 
erately elevated crurum. 


Description: Medium-sized Pododesmus, reaching 24 mm 
in height, ovate, slightly inequivalved with left (free) valve 
more inflated, slightly inequilateral, beaks central, shell 
thin. Left valve with approximately 15 to 17 low, some- 
what irregular radial ribs; interior margin of valve flat- 
tened. Right valve with attachment scar covering anterior 
one-fourth of valve, remainder of valve with approximately 
15 to 17 radial ribs, spinose near ventral margin of valve. 
Radial ribs smaller and more crowded anteriorly. Right 
valve with small byssal foramen, encircled by a low rim; 
lower half of byssal foramen plugged by a calcareous de- 
posit. Foramen situated beneath and immediately adjacent 
to a moderately elevated crurum (= chondrophore). Cru- 
rum with a narrow slot for resilium. Interior of right-valve 
margin somewhat flattened. 


Holotype: LACMIP 11515. 
Type locality: CSUN loc. 1511, 47°44'45"N, 122°51'06"W. 


Paratypes: LACMIP 12227-12229; all from CSUN loc. 
ISL. 


Dimensions: Of holotype, height 20.9 mm, length 18.1 
mm; paratype 12227, height 16 mm, length 14.5 mm; 
paratype 12228, height 24 mm, length 20 mm; paratype 
12229, height 17 mm, length 16 mm. 


Discussion: The new species is assigned to Pododesmus s.s. 
on the basis of the combination of the following features: 
radial sculpture on both valves, small plugged byssal fo- 
ramen, and the unnotched dorsal margin of the relatively 


Page 271 


Seattle 
Washington 


in ©) 
9 
Q, 
= 
19 
| Oo 
4 is) 
| 
| © 
S) 


Figure 1 


Location map for localities of Pododesmus (Pododesmus) dun- 
hamorum Squires, sp. nov. 


thick right valve. The new species is remarkably similar 
to Pododesmus (P.) decipiens, the type species of Pododesmus 
s.s., and especially to specimens (LACM 78-95, LACM 
78-96) of the type species from Golfo San Jose, Chubut 
Province, Argentina. OLSSON & PETIT (1964:529-530, pl. 
77, fig. 1) gave a detailed description of Pododesmus (P.) 
rudis (Broderip, 1834), the junior subjective synonym of 
P. (P.) decipiens, and figured the interior of the right valve. 
CARCELLES (1941:pl. 1, figs. 1, 2) and KEEN (1969:fig. 
C103 12a, b) also provided illustrations of P. (P.) rudis. 
The shell of Pododesmus is morphologically similar to 
that of Anomia Linné, 1758, the main distinction being 
that Pododesmus has two muscle scars in the central ‘“‘white 
area” on the interior of the left valve rather than three, as 
in Anomia (BEU, 1967; KEEN, 1969). Also, in Pododesmus 
both valves are radially sculptured, opaque, and fairly 
thick, whereas in Anomia the right valve lacks radial sculp- 
ture and both valves are translucent and usually thin (BEU, 
1967). Pododesmus is further distinguished by a byssal 
foramen that may be partially or entirely closed and which 
does not open as a slit at the dorsal margin, and a byssal 
plug that may be retained within the foramen (BEU, 1967; 
KEEN, 1969). Although the muscle scars on the left valve 
are not preserved in the new species, the overall mor- 


Page 272 


The Veliger, Vol. 36, No. 3 


Explanation of Figures 2 to 9 


Figures 2-9. Pododesmus (Pododesmus) dunhamorum Squires, sp. nov., CSUN loc. 1511. Figures 2-3: paratype, 
LACMIP 12227, left valve, x 2.6; Figure 2, exterior; Figure 3, interior. Figures 4-7: holotype, LACMIP 11515, 
right valve, x 2.5; Figure 4, exterior; Figure 5, interior; Figure 6, dorsal view of hinge line; Figure 7, anterior 
view. Figure 8: paratype, LACMIP 12228, right-valve interior, x 2.2. Figure 9: paratype, LACMIP 12229, right- 


valve interior, x 2.4. 


phology of both valves is in keeping with features of Po- 
dodesmus rather than of Anomuia. 

Pododesmus is anatomically the most primitive living 
anomiid (YONGE, 1977, 1980), and it probably evolved 
into Anomia (YONGE, 1977). Using shell microstructure of 
primarily the right valve, CARTER (1990) subdivided the 
anomiids into three groups. The only species of Pododesmus 
that he studied was the living Pododesmus (Monia) macro- 
chisma (Deshayes, 1839), and he included it among the 
“Anomia simplex group” that is characterized by a right 
valve with an outer layer of calcitic simple prisms and 
inner layers of aragonite and a left valve that always has 
a prominent layer of foliated structure. This group rep- 
resents a primitive microstructure grade that is compatible 
with the primitive soft anatomy of P. (M.) macrochisma 
(CARTER, 1990). 

KEEN (1969) recognized four subgenera in Pododesmus: 
Pododesmus s.s., Monia Gray, 1850, Heteranomia Winck- 


worth, 1922, and Tedinia Gray, 1853. The only two sub- 
genera with a known fossil record are Pododesmus s.s. and 
Monza. KEEN (1969) distinguished these two genera on the 
basis of the size of the byssal foramen, with Pododesmus 
having a much smaller one. HERTLEIN & GRANT (1972) 
reported Pododesmus as having thicker valves and a smaller 
foramen than Monza, and that the foramen is always plugged 
in Pododesmus but is usually open in Monza. BEu (1967) 
considered Monza to be a distinct genus and not a subgenus 
of Pododesmus. He noted that the right valve of Pododesmus 
is considerably thicker than the very thin right valve of 
Moma and that the byssal plug is small and permanently 
fused into the shell in Pododesmus, whereas in Monza the 
byssal plug is large, thin, and completely free. Further, in 
Pododesmus the crurum is approximately triangular, with 
anterior and posterior dorsal resilial surfaces, whereas in 
Monza the crurum has only a single dorsal resilial surface. 
Although the crurum of the new species is not well pre- 


R. L. Squires, 1993 


served and is incomplete even on the holotype, the other 
morphologic features indicate placement in Pododesmus s:s. 
rather than in Monza. 

The new species is similar to Pododesmus paucicostatus 
Bev (1967:240, pl. 1, fig. 3; pl. 2, figs. 6, 9, 10; text-figs. 
2a, d) from the middle Miocene of New Zealand (BEU 
& MAXWELL, 1990). Beu’s species has all the diagnostic 
features of Pododesmus s.s. and is judged herein to be as- 
signable to Pododesmus s.s. The new species differs from 
Beu’s species in the following features: smaller valve size, 
thinner valves, and smaller byssal foramen. 

The new species is also similar to Paranomia scabra 
(Morton, 1834; WADE, 1926:67-68, pl. 22, figs. 3-9) 
from Upper Cretaceous strata in the southeastern part of 
the United States. The new species, however, is smaller, 
it has coarser and more closely spaced radial ribs, and a 
byssal foramen is located much closer to the crurum and 
lacks the long linear scar between the foramen and the 
crurum. 

Only two other Eocene anomiids are known from the 
Pacific coast of North America. One is Pododesmus inor- 
natus (GABB, 1864:217, pl. 32, figs. 288, 288a) from the 
middle Eocene in central California and southwestern 
Washington (STEWART, 1930; VOKEs, 1939; WEAVER, 1942 
[1943]; KEEN & BENTSON, 1944; Moore, 1987). VOKES 
(1939:57-58, pl. 3, figs. 6, 7, 9, 11) assigned P. inornatus 
to Pododesmus (Monia). Only one of the figured specimens 
(UCMP hypotype 15587, see VOKEs, 1939:pl. 3, fig. 6) 
shows the interior of the right valve of P. inornatus. The 
byssal foramen and crural area are very similar to that of 
the new species, and I believe that P. inornatus should be 
placed in Pododesmus s.s. and not in Monza. The only other 
figured specimen of P. inornatus that shows the byssal 
foramen area is UCMP hypotype 15589 (see VOKES, 1939: 
pl. 3, fig. 11), but only the exterior of the right valve is 
free of matrix. Vokes’ illustration is misleading because it 
gives the impression that the foramen is free of matrix. 
The area around the foramen has been excavated, and the 
border of the foramen is no longer present. It is impossible 
to tell what the exact diameter of the foramen was, and 
the larger diameter may be an artifact. Nevertheless, the 
foramen is smaller than that normally present on speci- 
mens of Monza. Pododesmus (P.) dunhamorum differs from 
Pododesmus (P.) inornatus (Gabb, 1864) in having a less- 
inflated left valve, fewer but much stronger radial ribs on 
the left valve, an ornamented right valve, and in lacking 
commarginal riblets or lamellae on the left valve. 

The other reported Eocene anomiid from the Pacific 
coast of North America is Anomia mcgoniglensis HANNA 
(1927:278, pl. 31, figs. 1, 2, 5, 7), from middle Eocene 
(‘“Domengine Stage’’) strata of the San Diego area, south- 
ern California, to southwestern Oregon (KEEN & BENTSON, 
1944; TURNER, 1938; WEAVER, 1942 [1943]; GIVENS & 
KENNEDY, 1976; SQUIRES, 1984, 1989; MoorE, 1987). 
VOKES (1939) questionably put A. mcgoniglensis into syn- 
onymy with Pododesmus (Monia) inornatus because the 
range in coarseness of sculpturing in A. mcgoniglensis over- 


Page 273 


laps with that observed in P. (M.) inornatus. GIVENS & 
KENNEDY (1976), however, established A. mcgoniglensis as 
a species of Anomia, on the basis of well-preserved left 
valves that show three, rather than two, muscle scars. 

The only other Pacific coast of North America Paleogene 
anomiid species that has been assigned to Pododesmus sensu 
lato is P. newcombe1 CLARK & ARNOLD (1923:141, pl. 21, 
figs. 3-6; WEAVER, 1942 [1943]: 100-101, pl. 23, figs. 2, 
3, 5) from the upper Oligocene Sooke Formation, on south- 
ern Vancouver Island, British Columbia. The interior of 
this species is unknown, but P. (P.) dunhamorum differs 
from it by having a much flatter right valve, coarser radial 
ribs, and fewer and more widely spaced radial ribs. CLARK 
& ARNOLD (1923) noted that P. newcombei is similar to 
P. macrochisma (Deshayes, 1839) [= P. cepio (Gray, 1850)]. 
Modern workers assign Deshayes’ species to the subgenus 
Mona. Pododesmus (Monia) macrochisma ranges today along 
the Pacific coast of North America and in Japan, and is 
known as a fossil from rocks as old as late Miocene (MOORE, 
1987). 

By late Eocene, Pododesmus s.l. was present in New 
Zealand, and Pododesmus s.s. lived there from Oligocene 
through middle Miocene (BEu, 1967; BEU & MAXWELL, 
1990). IHERING (1907) reported four species of Pododesmus 
from the Patagonian Formation in Patagonia, southern 
Argentina, and Davies (1975) considered this formation 
to be early Miocene in age. HERTLEIN & GRANT (1972), 
however, concluded that Ihering’s generic assignment of 
his four species is tenuous because of their poor preser- 
vation. Pododesmus (P.) rudis has been reported from Plio- 
cene rocks in Venezuela (WEISBORD, 1964). Pododesmus 
s.l. was present along the Gulf Coast of North America 
by the early Pleistocene (OLSSON & PETIT, 1964; WARD 
& BLACKWELDER, 1987) and today persists there as P. (P.) 
rudis, which also lives in the West Indies and along much 
of the western Atlantic coast of South America. GARDNER’S 
(1926) report of P. (P.) rudis from the upper lower Mio- 
cene Chipola Formation in Florida and a report of this 
species from the lower Pleistocene Waccamaw Formation 
in North Carolina could not be substantiated by WEISBORD 
(1964) and WARD & BLACKWELDER (1987), respectively. 

The geologic range of Pododesmus s.s., previously re- 
ported as Miocene to Recent (KEEN, 1969; DaviEs, 1971), 
is emended herein as late early Eocene to Recent. 


Etymology: The species is named for George and Cressie 
Dunham, whose cooperation made the discovery of this 
new species possible. 


Distribution: Upper lower Eocene (near boundary be- 
tween “Capay Stage” and ‘“Domengine Stage’), upper 
Crescent Formation, west side of Dabob Bay, eastern 
Olympic Peninsula, Jefferson County, western Washing- 
ton (CSUN locs. 1502, 1511, and 1512). 


ACKNOWLEDGMENTS 


George and Cressie Dunham (Pulali Point, Washington) 
kindly allowed access to private property in the Pulali 


Page 274 


Point area (CSUN locs. 1511 and 1512) and made this 
and other studies possible. Most of the specimens of the 
new species were collected by James L. and Gail H. Goe- 
dert (Gig Harbor, Washington) and Keith L. Kaler 
(Olympia, Washington). Ross E. and Marion Berglund 
(Bainbridge Island, Washington) provided some of the 
specimens from CSUN loc. 1502. 

David R. Lindberg (UCMP) loaned specimens of com- 
parative material. LouElla R. Saul (LACMIP) allowed 
access to the collections and loaned specimens of Paranomia 
scabra. Lindsey T. Groves and C. Clifton Coney (LACM) 
allowed access to modern specimens of anomiids. Lindsey 
T. Groves, George K. Kennedy (LACMIP), and Richard 
E. Petit (North Myrtle Beach, South Carolina) provided 
some key literature. James L. Goedert read an early ver- 
sion of the manuscript. George L. Kennedy and an anon- 
ymous reviewer critically read the manuscript. 


LOCALITIES CITED 


CSUN loc. 1502. From boulder-sized blocks within a mod- 
ern landslide block at base of a steep hillside, 2 km S 
of Quilcene on W shore of Dabob Bay just S of latitude 
47°47'30"N, NE, section 36, T27N, R2W, U.S. Geo- 
logical Survey, 7.5-minute, Quilcene, Washington 
quadrangle, 1953, eastern Olympic Peninsula, Jefferson 
County, Washington. Upper Crescent Formation. Age: 
Late early Eocene (near boundary between ‘“Capay 
Stage” and ‘““‘Domengine Stage’”’). Collectors: J. L. Goe- 
dert, R. E. and M. Berglund, 1991. 

CSUN loc. 1511. Pebble conglomerate, 63 m above base 
of stratigraphically lowermost sedimentary interbed 
found along seacliff on west side of Dabob Bay at Pulali 
Point, latitude 47°44'45”N, longitude 122°51’06’W, 
central part of section 18, T26N, R1W, U.S. Geological 
Survey, 7.5-minute, Seabeck, Washington quadrangle, 
1953 (photorevised 1968), eastern Olympic Peninsula, 
Jefferson County, western Washington. Upper Crescent 
Formation. Age: Late early Eocene (near boundary be- 
tween “Capay Stage” and “Domengine Stage’’). Col- 
lectors: J. L. and G. H. Goedert and K. Kaler, 1989- 
1991. (See SQuIREs et al., 1992:figs. 2, 3). 

CSUN loc. 1512. Same as the CSUN loc. 1511, except 
106 m stratigraphically higher in section. 


LITERATURE CITED 


ABBoTT, R. T. 1974. American Seashells—The Marine Mol- 
lusks of the Atlantic and Pacific Coasts of North America. 
2nd ed. Van Nostrand Reinhold Company: New York. 663 
pp., 24 pls. 

Beu, A. G. 1967. Notes on Australasian Anomiidae (Mollusca, 
Bivalvia). Transactions of the Royal Society of New Zealand, 
Zoology 9(18):225-243, pls. 1-2. 

Beu, A. G. & P. A. MAXWELL. 1990. Cenozoic Mollusca of 
New Zealand. New Zealand Geological Survey, Paleonto- 
logical Bulletin 58:1-518, pls. 1-57. 

BropeRip, W. J. 1834. [Notes on the] Genus Placuanomuia. 


The Veliger, Vol. 36, No. 3 


Proceedings of the Zoological Society of London [for 1834], 
Btr2:2=3° 

CARCELLES, A. 1941. Pododesmus de la Argentina y Uruguay. 
Physis (Revista de la Sociedad Argentina de Ciencias Na- 
turales) 19:5-10, pls. 1-2. 

CarTER, J.G. 1990. Evolutionary significance of shell micro- 
structure in the Palaeotaxodonta, Pteriomorpha and Isofili- 
branchia (Bivalvia: Mollusca). Pp. 135-296, figs. 1-60, charts 
1-9. In: J. G. Carter (ed.), Skeletal Biomineralization: Pat- 
terns, Processes and Evolutionary Trends. Vol. 1, text; Vol. 
2, atlas and index, 200 pls. Van Nostrand Reinhold Com- 
pany: New York. 

Cxiark, B. L. & R. ARNOLD. 1923. Fauna of the Sooke For- 
mation, Vancouver Island, with a description of a new coral 
by T. Wayland Vaughan. University of California Publi- 
cations, Bulletin of the Department of Geological Sciences 
14(5):123-234, pls. 15-42. 

Davigs, A. M. 1971. Tertiary Faunas—A Text-book for Oil- 
field Palaeontologists and Students of Geology. Vol. 1. The 
Composition of Tertiary Faunas. Revised and updated by 
F. E. Eames. George Allen & Unwin: London. 571 pp. 

Davies, A. M. 1975. Tertiary Faunas—A Text-book for Oil- 
field Palaeontologists and Students of Geology. Vol. 2. The 
Sequence of Tertiary Faunas. Revised and updated by F. 
E. Eames & R. J. G. Savage. George Allen & Unwin: 
London. 447 pp. 

DESHAYES, G. P. 1839. Nouvelles espéces de mollusques, prove- 
nant des cotes de la Californie, du Mexique, du Kamtschatka 
et de la Nouvelle-Zelande. Revue Zoologique, par la Societe 
Cuvierienne 2:356-361. 

Gass, W. M. 1864. Descriptions of the Cretaceous fossils. 
California Geological Survey, Palaeontology 1:55-243, pls. 
9-32. 

GARDNER, J. 1926. The molluscan fauna of the Alum Bluff 
Group of Florida. Part 1. Prionodesmacea and Anomalo- 
desmacea. U.S. Geological Survey Professional Paper 142- 
A:1-240, pls. 29-36. 

GIVENS, C. R. & M. P. KENNEDY. 1976. Middle Eocene mol- 
lusks from northern San Diego County, California. Journal 
of Paleontology 50(5):954-975, pls. 1-4. 

Gray, J. E. 1850. On the species of Anomiadae. Proceedings 
of the Zoological Society of London 17:113-124. 

Gray, J. E. 1853. A revision of the genera of some of the 
families of Conchifera or bivalve shells. Annals and Mag- 
azine of Natural History, Series 2, 11:33-44, 398-402. 

Hanna, M. A. 1927. An Eocene invertebrate fauna from the 
La Jolla Quadrangle, California. University of California 
Publications, Bulletin of the Department of Geological Sci- 
ences 16(8):247-398, pls. 24-57. 

HERTLEIN, L. G. & U.S. GRANT IV. 1972. The geology and 
paleontology of the marine Pliocene of San Diego, California 
(Paleontology: Pelecypoda). San Diego Society of Natural 
History Memoir 2 (Part 2B):135-409, pls. 27-56. 

IHERING, H. von. 1907. Les Mollusques fossiles du Tertiaire 
et du Crétacé Supérieur de l’Argentine. Anales del Museo 
Nacional de Buenos Aires 15, Serie 3°, 7:1-611, pls. 1-18. 

KEEN, A. M. 1969. Superfamily Anomiacea Rafinesque, 1815. 
Pp. N383-385, fig. C103, 1a-12b. In: R. C. Moore (ed.), 
Treatise of Invertebrate Paleontology, Pt. N. Mollusca 6 (1 
of 3). Geological Society of America and Kansas University 
Press: Lawrence, Kansas. 

KEEN, A. M. 1971. Sea Shells of Tropical West America— 
Marine Mollusks from Baja California to Peru. 2nd ed. 
Stanford University Press: Stanford, California. 1064 pp., 
22 pls. 


R. L. Squires, 1993 


KEEN, A. M. & H. BENTSON. 1944. Check list of California 
Tertiary marine Mollusca. Geological Society of America 
Special Papers 56:1-280, figs. 1-3. 

LINNE, C. 1758. Systema naturae per regna tria naturae. Editio 
10, reformata, Regnum animale. Vol. 1. Holmiae. 1327 pp. 

Moore, E. J. 1987. Tertiary marine pelecypods of California 
and Baja California: Plicatulidae to Ostreidae. U.S. Geo- 
logical Survey Professional Paper 1228-C:1-53, pls. 1-34. 

Morton, S. G. 1834. Synopsis of the organic remains of the 
Cretaceous group of the United States. Appendix. Catalogue 
of the fossil shells of the Tertiary formations of the United 
States, by T. A. Conrad. Philadelphia. 88 pp., 19 pls.; Ap- 
pendix, 8 pp. 

O.sson, A. A. & R. E. Petir. 1964. Some Neogene Mollusca 
from Florida and the Carolinas. Bulletins of American Pa- 
leontology 47(217):1-71, pls. 1-7. 

PuHiuippl, R. A. 1837. Pododesmus, ein neues Genus der Ace- 
phalen. Archiv fur Naturgeschichte 3(1):385-387, pl. 9, figs. 
la-d. 

RAFINESQUE, C. S. 1815. Analyse de la nature, ou tableau 
del’universe des corps organisées. Palmero. 224 pp. 

Rios, E. C. 1975. Brazilian marine mollusks iconography. 
Fundacao Universidade do Rio Grande Centro de Ciéncias 
do Mar Museu Oceanografico: Rio Grande, Brazil. 331 pp., 
91 pls. 

SQUIRES, R. L. 1984. Megapaleontology of the Eocene Llajas 
Formation, Simi Valley, California. Natural History Mu- 
seum of Los Angeles County, Contributions in Science 350: 
1-76, figs. 1-19. 

Squires, R. L. 1989. Middle Eocene rocky nearshore molluscs, 
Tejon Formation, Tehachapi Mountains, California [ab- 
stract]. Western Society of Malacologists, Annual Report 
21:18. 

Squires, R. L. 1992. New occurrences of the malleid bivalve 
Nayadina (Exputens) from the Eocene of Jamaica, Mexico, 
and Washington. The Veliger 35(2):133-136, figs. 1-6. 

Squires, R. L., J. L. GOEDERT & K. L. KALER. 1992. Pale- 
ontology and stratigraphy of Eocene rocks at Pulali Point, 
Jefferson County, eastern Olympic Peninsula, Washington. 


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Washington Division of Geology and Earth Resources, Re- 
port of Investigations 31:1-27, text figs. 1-7, pls. 1-3. 
STEWART, R. B. 1930. Gabb’s California Cretaceous and Ter- 
tiary type lamellibranchs. The Academy of Natural Sciences 

of Philadelphia, Special Publication 3:1-314, pls. 1-17. 

TuRNER, F. E. 1938. Stratigraphy and Mollusca of the Eocene 
of western Oregon. Geological Society of America Special 
Papers 10:1-130, figs. 1-7, pls. 1-22. 

VoKEs, H. E. 1939. Molluscan faunas of the Domengine and 
Arroyo Hondo Formations of the California Eocene. Annals 
of the New York Academy of Sciences 38:1-246, pls. 1-22. 

WADE, B. 1926. The fauna of the Ripley Formation on Coon 
Creek, Tennessee. U.S. Geological Survey Professional Pa- 
per 137:1-272, pls. 1-72. 

Warp, L. W. & B. W. BLACKWELDER. 1987. Late Pliocene 
and early Pleistocene Mollusca from the James City and 
Chowan River Formations at the Lee Creek Mine. Pp. 113- 
283, pls. 1-47. In: C. E. Ray (ed.), Geology and Paleontology 
of the Lee Creek Mine, North Carolina, I. Smithsonian 
Contributions to Paleobiology 61. 

WEAVER, C. E. 1942 [1943]. Paleontology of the marine Ter- 
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Washington, Publications in Geology 5 (Parts 1-3):1-789, 
pls. 1-104 [reprinted, 1958]. 

WEISBORD, N. E. 1964. Late Cenozoic pelecypods from north- 
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WINCKWORTH, R. 1922. Note on the British species of Anomia. 
Proceedings of the Malacological Society of London 22: 
23-26. 

YONGE, C. M. 1977. Form and evolution in the Anomiacea 
(Mollusca: Bivalvia)—Pododesmus, Anomia, Patro, Enigmo- 
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nov.). Philosophical Transactions of the Royal Society of 
London B, 276:453-527. 

YONGE, C. M. 1980. On Patro australis with comparisons of 
structure throughout the Anomiidae (Bivalvia). Malacologia 
20(1):143-151. 


The Veliger 36(3):276-284 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Relict Shells of Subantarctic Mollusca from the 


Orange Shelf, Benguela Region, off 


Southwestern Africa 


by 


JOHN PETHER 


South African Museum, P.O. Box 61, Cape Town 8000, South Africa 


Abstract. 


Subfossil shells of three locally extinct mollusk species of Subantarctic affinity have been 


found in sediments on the middle Continental Shelf (120-140 m depth) in the Benguela region off 
southwestern Africa. These are the venerid Tawera philomela (E. A. Smith), the ranellid Sassza (Sassia) 
philomelae (Watson), and the buccinid Pareuthria fuscata (Bruguiére). All three presently live on the 
mid-Atlantic islands of Tristan da Cunha and Gough. The abraded, bored, and encrusted state of 7. 
philomela shells, including algal borings, records their exposure as a shell gravel under high-energy 
conditions in the photic zone. Cores of sediments and a 'C date of 13.5 kyr B.P. confirm that 7. 
philomela abundantly populated coarse sands in the sample area during the low sea level (~ —100 m) 
of the late glacial. The shell condition of P. fuscata suggests it was a contemporary, while that of S. 
philomela indicates a higher position in the faunal succession of the sample area, most likely due to a 
greater depth preference. The dispersal of these species from the mid-Atlantic to Africa is consistent 
with glacial intensification of the circumpolar circulation and accords with previous work indicating 
enhanced opportunities for Southern Ocean dispersal during glaciations. This zonal dispersal compen- 
sates to some extent for Africa’s lack of shelf connections to the subpolar benthic fauna. The specific 
means of dispersal remains speculative, as do the causes for the subsequent local extinction of the 


dispersed species. 


INTRODUCTION 


The occurrence of submerged subaerial and shallow-water 
sediments, with enclosed fossils from terrestrial, estuarine 
and shoreface environments, is a widespread feature of the 
continental shelves of the world (EMERY, 1968). The deep- 
est of these relict sediments were deposited when sea level 
was lowered to about —130 m at the Last Glacial Max- 
imum, while the subsequent recovery of sea level left in 
its wake a transgressive sheet comprising sands and gravels 
abandoned on the deepening shelf. Radiocarbon-dated, very 
shallow-water molluscan shells from relict sediments have 
been useful in estimating the deglacial rise of sea level, 
while occurrences of “warm” and “cold” species beyond 
their modern ranges are evidence for fluctuations in the 
temperature of coastal waters over this period (EMERY ef 
al., 1988; TAVIANI et al., 1991). This paper documents the 
finding of shells of Subantarctic or Southern Ocean mol- 
lusks not previously recorded from the southwest African 


continental shelf (Figure 1). Taphonomic and stratigraph- 
ic evidence is presented, showing that the most common 
species, a venerid, is associated with relict coarse-grained 
sediments related to glacially lowered sea level. The dis- 
persal of the species over ~ 2900 km from the mid-Atlantic 
islands to the African coast is discussed. 


SOURCE or SAMPLES 


On the Orange shelf off the west coast of southern Africa 
(Figure 1a), the shoreline deposits of the deglacial trans- 
gression are to a large extent covered by a coast-parallel 
Holocene mudbelt (Figure 1b) consisting primarily of ter- 
rigenous silts and clays transported southward from the 
Orange River by a poleward undercurrent beneath the 
Benguela Current (ROGERS, 1977; ROGERS & BREMNER, 
1991). The mudbelt thins seaward, where it laps onto the 
middle shelf in the vicinity of the Last Glacial shoreline. 


ileeeether, 1993 Page 277 


Sylvia Hill 
#RC13-229 


Namibia | 


@TRISTAN 
DA CUNHA 


South 


Atlantic 


/ 
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' 


| ORANGE 


*Discovery 


South Africa 


CAPE TOWN 


Figure 1 


Figure 1a. West coast of southern Africa. Localities where Concholepas concholepas was obtained in Holocene beach 
sediments indicated by C. Figure 1b. Sample area off Kleinzee with bathymetry indicated at 10 m intervals and 
Holocene mudbelt shaded. Figure 1c. Southeast Atlantic Ocean showing mid-Atlantic islands, seamounts, and 3 
km isobath. McN = McNish Seamount; STC = Subtropical Convergence. 


There the coarse sands and gravels of the glacial shoreline 
are exposed or shallowly buried beneath the Holocene 
mud. The occurrence of these relict sediments was dis- 
cussed by ROGERS (1977), who noted the presence of grain 
surface features typical of littoral sands. More recently, 
exploration of this terrain for diamonds has produced a 
suite of samples of dredged shells, made available courtesy 
of De Beers Marine (Pty) Limited and deposited in the 
South African Museum (SAM). Fifty-three samples were 
taken in an area off Kleinzee (Figure 1b). Bulk samples 
of shell were collected onboard the prospecting vessel, from 
the screens that exclude coarse gravel from the heavy- 
mineral concentration process. Additional specimens, 
mainly less common species, were also individually selected 
from the gravel screens. Taxa present in the bulk samples 
were identified, sorted, and counted. Documentation of the 
entire assemblage recovered, including methods of analysis, 
will be presented elsewhere (in preparation). Observations 
on shell condition were also made. A reconnaissance of the 
endolithic taxa infesting shells was accomplished by im- 
pregnating shells with polyvinylbutyrol (PVB) in acetone 
under low vacuum, then dissolving the shells in dilute HCl 
to reveal the cast borings. Relevant initial results are dis- 
cussed here. 


THE SUBANTARCTIC MOLLUSCA 
Tawera philomela (E. A. Smith, 1885) 


This venerid (Figure 2a-c) is the most abundant bivalve 
recovered from the sample area (34.4% of total bivalves). 
Tawera philomela occurs at the Southern Ocean islands of 
Tristan da Cunha, Gough, and South Georgia. A species 
of Tawera occurs on the west and east coasts of South 
America south of approximately 35°S, and at the Falkland 
Islands. Two species occur in southern Australia, two in 
New Zealand, and five species are distributed around the 
Subantarctic islands near New Zealand (DELL, 1964). 
New Zealand, with nine fossil species ranging from the 
Miocene, is evidently the distributional center of the genus 
(DELL, 1964). The record of 7. philomela from South 
Georgia is mentioned only by DELL (1964), but because 
the molluscan fauna of this locality is Antarctic in character 
(POWELL, 1965), it should be viewed with some suspicion. 

Tawera philomela has been recorded from a large range 
of depths: off Tristan at 7-12 m, 8-45 m, 117-104 m, and 
1800 m (DELL, 1964; SooT-RYEN, 1960; SMITH, 1885); 
off Nightingale Island at 180-280 m (SMITH, 1885); and 
off Gough at 90-140 m, 180 m, and 22 m (DELL, 1964; 
MELVILL & STANDEN, 1907, South African Museum Col- 


Page 278 


The Veliger, Vol. 36, No. 3 


Figure 2 


Figure 2a-c. Tawera philomela. Figure 2a. Exterior right valve. Figure 2b. Interior left valve. Figure 2c. Interior 
right valve (SAM-PQ 2681a, b). Figure 2d. Sassza (Sassia) philomelae (SAM-PQ 2682a, b, c). Figure 2e. Pareuthria 
fuscata (SAM-PQ 2683a, b, c). Figure 2f. Abraded exterior of 7. philomela valve showing unroofed Entobia borings 
(large holes) and Penetrantia borings (tiny “‘pinprick” holes) (SAM-PQ 2684a). Interior of 7. philomela valve 
showing Spathipora boring (arrowed) and encrusting bryozoans and serpulids (SAM-PQ 2684b). All scale bars are 


10 mm. Material deposited in South African Museum. 


lections). The very deep record (1800 m) was evidently 
empty shells (SOOT-RYEN, 1960), and these were probably 
transported down the steep submarine slopes of Tristan. 


Sassia (Sassia) philomelae (Watson, 1880) 


Although this ranellid (Figure 2d) was not present in the 
bulk shell samples, numerous specimens were collected by 
De Beers personnel from shell trapped on the gravel screens. 


Sassia philomelae is recorded from Nightingale Island, near 
Tristan da Cunha (WATSON, 1886; BEU, 1985), where it 
was collected in depths of 180 to 280 m. The genus is not 
confined to Subantarctic waters and most species occur in 
the southwest Pacific (Australasia) (BEU, 1985), although 
the S. remensa (Iredale) species group occurs throughout 
the tropical western Pacific, and S. nassariformis (G. B. 
Sowerby III) occurs off southeast Africa and in the western 
Indian Ocean. 


ebether 1998 


Pareuthria fuscata (Bruguiére, 1789) 


A few specimens of this buccinid (Figure 2e) are present 
in the bulk samples and numerous examples were collected 
from the screens. The species is recorded from the Strait 
of Magellan and the Falkland Islands (POWELL, 1954). 
Material in the South African Museum collected from 
Gough Island includes this species and represents a new 
distributional record. SMITH (1885) mentions a record from 
Kerguelen. The genus is characteristic of Subantarctic and 
Antarctic waters, and several species are distributed from 
a center in the Magellanic region eastward to Kerguelen, 
the Davis and Ross seas, and the Subantarctic islands south 
of New Zealand (POWELL, 1954). It has been collected 
from the intertidal to 46 m (SMITH, 1885; POWELL, 1954; 
South African Museum Collections). 

These three species have not previously been recorded 
from the African coast. However, an assemblage from the 
Namibian shelf off Sylvia Hill (Figure 1a) contained some 
shallow-water, relict components (ROGERS, 1977; ROGERS 
& BREMNER, 1991). A doubtful record in this fauna was 
Pitar callicomatus (Dall, 1902), otherwise known from only 
a few specimens from tropical west America (KEEN, 1971). 
Material from off Sylvia Hill, supplied by M. Bremner, 
confirmed that Tawera philomela was present. Misidenti- 
fication of 7. philomela seems to have been the source of 
the erroneous report of P. callicomatus. 

The extant molluscan fauna of the Namaqua Province 
on the southwest coast of Africa does contain a Southern 
Ocean component (e.g., Choromytilus, Aulacomya, Argo- 
buccinum), and it is therefore insufficient to argue that 
shells of Southern Ocean species are locally extinct because 
they have been recovered from a relict sediment tract. The 
input of Subantarctic water into the Benguela Current 
system is sporadic, but substantial (SHANNON ef al., 1989) 
and the islands of Tristan and Gough straddle the Sub- 
tropical Convergence along which this input is sourced. 
The apparent depth ranges of the species do not preclude 
them from the depths where collected, except possibly Pa- 
reuthria fuscata, and an ability to populate a large depth 
range may be advantageous for species inhabiting the areally 
limited, shallow shelves of steep oceanic islands. There is 
no marked contrast in temperature between the islands of 
Tristan and Gough and the Orange Shelf, and a relict 
sediment terrain may be the likely habitat of Subantarctic 
taxa extending their ranges equatorward by submergence. 
However, additional evidence presented below supports 
the geologically relict nature of these shells. 


EVIDENCE FOR RELICT OCCURRENCE 


Shell Taphonomy of Tawera 


The valves of Tawera philomela from the Orange Shelf 
are abraded to various degrees, bored by endolithic organ- 
isms, and encrusted by epilithic taxa. Macroborings rep- 
resent the ichnogenus Entobia Bronn, 1838, which is pro- 
duced by boring sponges, particularly the Clionidae. The 


Page 279 


clionid borings have papillar openings on both sides of the 
valve, indicating postmortem infestation (BROMLEY, 1970). 
Smoothed valve exteriors with unroofed Entobia are com- 
mon (Figure 2f) and attest to an abrasive environment. 
Dissolution was a minor factor, as is evident in the good 
preservation of Entobia wall microsculpture and unetched, 
well-preserved valve interiors. 

The largest microborings are visible to the eye as “‘pin- 
pricks” and are always most densely concentrated on the 
valve exteriors (Figure 2f). Abraded valve surfaces and 
PVB casts reveal connecting stolons between pits, confirm- 
ing their bryozoan origin and a morphology attributable 
to Penetrantia Silen, 1946. Another boring bryozoan, Spa- 
thipora Fischer, 1866, almost exclusively colonized valve 
interiors (Figure 2g). Several species of unilaminar, chei- 
lostome bryozoans occur in valve interiors, with very few 
exterior occurrences. Similarly, encrusting serpulid poly- 
chaetes, mainly Spirorbis spp., occur in valve interiors (Fig- 
ure 2g). No Tawera valves with preserved ligamental ma- 
terial were observed. Fresh 7. philomela valve interiors 
have an orange hue. This color is not preserved or is very 
faint in most Orange Shelf specimens, and specimens with 
the best color retention are still faded in comparison with 
fresh specimens from Gough Island. 

The PVB casts reveal dense “mats” of microboring be- 
tween the larger sponge and bryozoan borings and these 
“mats” are best developed in valve exteriors. This micro- 
boring is attributable to endolithic algae and fungi, but 
the relatively large size of most of the borings (~25 wm 
diameter) suggests an algal origin. 


Interpretation: Clionid borings occur in both shallow and 
deep settings and indicate conditions of low sedimentation 
(EKDALE et al., 1984), but a rich assemblage of sponge 
borings indicates a depth less than 100 m (BROMLEY, 1970). 
NELSON et al. (1988) have produced a simplified classifi- 
cation of bryozoan growth forms to facilitate their appli- 
cation to palaeoenvironmental studies. Unilaminar en- 
crusting forms, such as those present within 7awera shells, 
are typical of moderate to high current energy and low 
sedimentation rates, and are most common at inner-shelf 
depths. The sedentary polychaetes Spirorbis spp. are dom- 
inantly intertidal to shallow shelf (Day, 1967). 

Notably, Penetrantia preferentially infested valve exte- 
riors, while Spathipora, spirorbids, and encrusting bryo- 
zoans are almost invariably situated in the interior of the 
valves. This marked partitioning of the concavo-convex 
shell substratum suggests that most 7awera shells were 
exhumed after death by physical reworking of the sediment 
and deposited in convex-up, hydrodynamically stable ori- 
entations. A similar phenomenon has been documented in 
detail from bivalves of the Plio-Pleistocene Red Crag by 
BisHop (1988), who concluded that the encrusting bryo- 
zoan Cribrilina exploited the concavities of convex-up shells 
as a refuge in high-energy environments, the larval settle- 
ment behavior apparently being specialized for concavo- 
convex bivalve substrata. In contrast, valves on the deeper 


Page 280 


shelf most often lie in a concave-up position due to the 
absence of strong currents and activity of carnivores, scav- 
engers, and bioturbation (EMERY, 1968). 

The distinction of endolithic algal microborings from 
borings made by light-independent fungi is difficult due 
to size and morphological overlap (GOLUBIC et al., 1975). 
However, in a complex substratum with dark and illu- 
minated surfaces, their distributions will be characteris- 
tically different (EKDALE et al., 1984). The fact that the 
microboring is intensely developed in the exteriors of 7a- 
wera valves is consistent with an algal origin. PERKINS & 
HALSEY (1971), examining shells from relict Carolina shelf 
sediments, found the zone of high algal boring activity to 
extend to a depth of ~25 m. Two parallel zones located 
offshore with high incidence of algal boring were inter- 
preted as relict Pleistocene sediments. In clear tropical 
waters endolithic algae are concentrated shallower than 
30 m (ROONEY & PERKINS, 1972; PERKINS & TSENTAS, 
1976). Thus, although microboring algae may occur to the 
limits of light penetration (200-250 m in very clear water), 
an ichnocoenose that includes abundant algal boring is a 
useful indicator of inner-shelf palaeodepths. 

The abraded, bleached, and bioeroded condition of 7a- 
wera shells contrasts strikingly with the condition of bi- 
valves in the same samples that are expected to occur in 
the sample area at present. The valves of Tellina gilchristi, 
Lucinoma capensis, and Dosinia lupinus are much better 
preserved, some have vestigial ligamental material, and the 
relatively few examples that have been subjected to deg- 
radation from exposure at the seabed show dissolution 
effects rather than abrasion. Encrusting and endolithic 
bryozoa are absent, suggesting that they are characteristic 
of shallow water in this shelf region. Significantly, micro- 
boring is on a finer scale than by Tawera (borings 3-4 um 
diameter) and numerous spherical sporangial bodies are 
present, indicative of a fungal origin (PERKINS & HALSEy, 
1971; ROONEY & PERKINS, 1972; PEEBLES & LEWIS, 1988). 
BROWN & HEnrRy (1985) record the depth of the 1% light 
level in the southern Benguela region as being from 20 to 
30 m, with penetration to 40 m in newly upwelled, phy- 
toplankton-poor water. Doubling of this penetration to 
compensate for sea-level change is still ~40 m short of the 
shallowest samples. Thus the probability of the expected 
Holocene species having been exposed to significant light 
levels is very low, supporting the fungal origin of their 
microboring facies. The contrast in microboring facies be- 
tween 7awera and expected Holocene species further sup- 
ports a mainly algal origin for the microboring in the 
former. 

In summary, the abraded state and the identity and 
distributions of epi- and endolithic taxa in Tawera valves 
records their exposure on the sea floor as a shelly gravel 
subjected to current activity within the photic zone. An 
inner-shelf palaeoenvironment is inferred and indicates 
that the occurrence of 7. philomela is relict from a period 
when shallow water pertained over the sample area. How- 
ever, the good preservation of the taphonomic features 


The Veliger, Vol. 36, No. 3 


formed at inner-shelf depths, as well as the occurrence of 
a minority of very well-preserved valves, indicates that 
most valves were buried and “stored” in shallow-water 
sediments. Because the stringent definition of relict occur- 
rence refers to material (sediments and shells), exposed on 
the seabed, which is “out of place” in the modern envi- 
ronment, these buried shells are not, for the most part, 
strictly relict. However, a minor portion of abraded, bored 
Tawera valves have superimposed the dissolution and mi- 
croboring features found on deep-water taxa. These valves 
indicate continued exposure at the sediment surface as 
depths increased over the sample area and apparently re- 
sided on the top of the bed of shallow-water sediments. 
This superimposition of the deep-water taphofacies iden- 
tifies the particular valves that remained on the sediment 
surface as relict shells for some time. 


Sediment Cores 


Stratigraphic confirmation of the taphonomic observa- 
tions was provided by the subsequent recovery of vibracores 
of sediments from the sample area. These revealed that 
the postglacial sedimentary sequence in the sample area 
is condensed due to low sedimentation rates. The Tawera 
valves occur in a gravelly, coarse, polished sand along with 
worn mytilid and barnacle fragments. Tawera valves at 
the top of the unit have the deep-water taphofacies su- 
perimposed. This shallow-water unit, ~0.15 to 0.6 m thick, 
is overlain by sandy, glauconite-bearing, green mud, vary- 
ing in thickness from ~0.2 to 1.0 m, which encloses the 
modern taxa of the area. The 7awera-bearing, coarse sand 
likely continues landward as a transgressive sand sheet 
beneath the overlying mud, which thickens landward into 
the Holocene mudbelt lens (ROGERS, 1977). 


Dating 


A radiocarbon date (Pta-5069) of 13,530 + 230 '*C yr 
B.P. (400 yr subtracted for the age of seawater) was ob- 
tained from particularly well-preserved shells of Tawera 
philomela from ~ —130 m depth in the sample area (J. C. 
Vogel, personal communication). The sea-level record ob- 
tained from dated corals off Barbados (FAIRBANKS, 1989) 
indicates an early deglacial sea level at ~ —100 m at this 
time. This supports the suggestion that the 7awera-bearing 
coarse sands are inner-shelf deposits, rather than shoreface 
deposits, and these shallow-shelf sands were rapidly aban- 
doned during the subsequent sea-level surge of the initial, 
major melt-water episode centered at ~12 'C kyr B.P. 
(FAIRBANKS, 1989). 

This date may be compared with the 15-11 “C kyr 
B.P. spread of dates on cold-water taxa equatorward of 
the modern ranges on the North American Atlantic shelf 
(EMERY e¢ al., 1988) and the late glacial 12-13.5 “C kyr 
B.P. cluster of ages of “Boreal Guests” from the southern 
European Atlantic shelf (TAVIANI et al., 1991). Another 
venerid found equatorward of its modern range in late 
glacial deposits is recorded from the Mauritanian shelf. 


iether 993 


This is Venus striatula, dated between 13 and 15 '*C kyr 
B.P., and suggested to correlate with a stronger, south- 
ward-shifted, cold Canary Current (PARK & FUTTERER, 
1989). 


The Subantarctic Gastropods 


Although examples of Pareuthria fuscata and Sassia phi- 
lomelae were poorly represented and absent, respectively, 
in the shell bulk samples, the fact that they are locally 
abundant at certain dredge sites (M. Mittelmeyer, personal 
communication) suggests that local factors of sedimentary 
history and facies preservation have determined their oc- 
currence. This may result from the a prior: influence of 
different environmental preferences of the species. By im- 
plication, their taphonomic signature may differ from that 
of a shallowly infaunal bivalve populating the coarse, pe- 
riodically mobile, inner-shelf substratum. Because the ma- 
jority of the available specimens were hand selected from 
the screens, rather than obtained arbitrarily by bulk sam- 
pling, there may also be a bias in observations on their 
taphonomic state. Nevertheless, it is significant that al- 
though relatively few specimens of Pareuthria fuscata are 
abraded, they resemble 7awera in that many were densely 
infested by Penetrantia and some contain encrusting bryo- 
zoa and spirorbids within apertures. Together with their 
evidently shallow-water environmental preference, this 
would suggest penecontemporaneity with Zawera. In con- 
trast, the shells of Sassia philomelae are not abraded and 
only a minority were lightly infested by Penetrantia, but 
all are bleached, all show corrosion effects, and most ex- 
hibit a pattern of biogenically mediated shell loss resem- 
bling that found on expected, deep-water Holocene taxa. 
Exhumation under deep-water conditions by bioturbation 
cannot account for this condition, as a preceding, shallow- 
water taphonomic signature is lacking and the exhumation 
of practically all specimens is very improbable. This species 
may have arrived on the African coast at a later time than 
Tawera and Pareuthria, or it persisted on the deepening 
shelf for a considerable time. The last is preferred as the 
more parsimonious alternative, the condition of S. philo- 
melae being due to a greater depth preference than the 
other Subantarctic representatives, leading to a taphonomic 
signature characteristic of taxa higher in the faunal suc- 
cession of the sample area. Additional radiocarbon dating 
would shed more light on this aspect. The possibility that 
S. philomelae is an undiscovered inhabitant of the deeper 
shelf off southwestern Africa cannot be excluded. 


DISCUSSION 


Presuming that Tawera philomela larvae drifted to the 
southern African west coast from Tristan da Cunha and/ 
or Gough islands, the factors facilitating this ~2900 km 
journey must be considered. A drift card released in the 
vicinity of Tristan da Cunha took six months to traverse 
the distance to the Cape coast at a rate calculated at 17 
cm/sec (SHANNON et al., 1973). Mean surface drift rates 


Page 281 


for cards and buoys between latitudes 30° to 40°S are less, 
varying from 10 to 15.5 cm/sec, while in the “Roaring 
Forties” rates of 15 to 20 cm/sec apply (LUTJEHARMS et 
al., 1988). The absence of modern 7. philomela on the 
southern African coast suggests that its larval stage is too 
short relative to prevailing drift rates to reach Africa. 

Sea-surface palaeotemperature estimates for the Last 
Glacial (~18 kyr B.P.) South Atlantic, based on radio- 
larians, indicate that Subantarctic waters were 2—5°C colder 
than today and Subantarctic isotherms were compressed 
due to a northward shift of the Polar Front toward an 
essentially stable Subtropical Convergence (MORLEY & 
Hays, 1979). This would have resulted in intensification 
of the atmospheric and ocean circulation, with cooler wa- 
ters being pumped northward through the Benguela region 
(Mor Ley & Hays, 1979). NEWELL e¢ al. (1981) estimated 
that the general increase in the intensity of the Last Glacial 
circulation of the Southern Hemisphere was about 17%. 
If applicable to the Westerlies, this is insufficient to shorten 
dramatically drift times from the mid-Atlantic to Africa. 

It is possible that the dispersal distance may have been 
interrupted by colonization of seamount summits (Figure 
1c), which would have been shallower during the Last 
Glacial. Seamounts McNish (—150 m) and RSA (—214 
m), although shallow, are too close to the source area to 
make an appreciable difference. Excessive depth renders 
the Walvis Ridge an unlikely route. Drift times to Vema 
(an island during the Last Glacial) may be shorter than 
to the African mainland, but larvae shed from there are 
more likely to drift north with the South Atlantic gyre 
than east toward the mainland. Colonization of Discovery 
(—329 m), at ~ —200 m depth at maximum sea-level fall 
and probably within the depth range of Tawera, would 
have shortened the traverse by about a third and this south- 
erly route has the advantage of faster drift rates. A role 
for seamounts, perhaps Discovery, cannot be discounted, 
but would ultimately require confirmation from the re- 
covery of shells. 

Significantly, eight of the ten bivalve species known from 
Tristan da Cunha have brood protection (SOoT-RYEN, 
1960). As remarked by SOOT-RYEN (1960), this is the safest 
means of propagation on an isolated island, because pelagic 
larvae would be carried away by currents before ready for 
bottom life. The maintenance of the population of Tawera 
philomela on the islands seemingly implies a short larval 
life. On the other hand, the prodissoconch is relatively 
large (up to 3 mm in height), and the distribution of Tawera 
species attests to successful long-distance dispersal on the 
geological time scale. Low temperatures and insufficient 
food are known to slow larval growth. For instance, the 
pelagic stage of Mytilus edulis is potentially more than 
doubled under these unfavorable conditions (LANE et al., 
1985). Furthermore, the pediveliger can delay metamor- 
phosis for up to six weeks in the absence of settlement 
surfaces (BAYNE, 1965). The species is also able to enter 
a second, post-larval pelagic stage by byssus rafting, and 
this ability is reported to be of widespread occurrence in 


Page 282 


bivalves, including a venerid (SIGURDSSON et al., 1976). 
The phenomenon has been examined in detail in Mytilus 
edulis, for which LANE et al. (1985) conclude that the 
potential pelagic existence could exceed six months. 

Without specific knowledge of the larval development 
of Tawera philomela, constraints within which to view its 
dispersal to Africa are lacking. If the larval stage lacks 
capabilities for prolonged drifting, a significant increase 
in glacial drift rates is required, or one must resort to the 
eventual possibility, in geological time, of a “sweepstakes” 
dispersal event such as the transport of juveniles nestled 
in the holdfasts of storm-dislodged kelp. The problem of 
dispersal may not equally apply to Sassia philomelae, be- 
cause tonnaceans have teleplanic larvae that can postpone 
metamorphosis for periods exceeding six months (SCHEL- 
TEMA, 1971). However, not all tonnaceans have equal 
ability in this regard and the restriction of S. philomelae 
to Tristan da Cunha and Gough islands suggests a short 
larval life. The dispersal problem is more acute for Pa- 
reuthria fuscata if, as with most buccinids, they hatch as 
crawling young from egg cases. This would suggest that 
the dispersal of P. fuscata must have been by way of rafting 
on flotsam, for instance on kelp fronds. Because sexes are 
separate, isolated incidences of rafting of individuals are 
unlikely to result in the establishment of large populations. 
Another means of rafting is provided by drift pumice from 
submarine volcanic eruptions (JOKIEL, 1990). Large mats 
of pumice are produced from mid-ocean volcanic ridges. 
A submarine eruption near Tristan produced a pumice 
mat, observed in 1725, that was 480 by 80 km in extent 
(FRICK & KENT, 1984). It is possible that larvae would 
settle on such material, with some ultimately making land- 
fall on the African coast. 

A further incidence of long-distance dispersal is the oc- 
currence of shells of the thaidid gastropod Concholepas 
concholepas in Holocene beach sediments in Namibia, just 
north of the Orange River (Figure 1a) (KENSLEY, 1985). 
The species is known from the Pliocene to Recent on the 
Peruvian and Chilean coasts of South America. The Na- 
mibian C. concholepas may be a chance pioneer population 
(KENSLEY, 1985), but additional specimens have recently 
been found much further south near the Olifants River 
(Figure 1a), in sediments infilling littoral gullies. Both 
finds may represent isolated populations from chance re- 
cruitment, but possibly were dispersed penecontempora- 
neously during the same unusual conditions. Although the 
larval life of Concholepas exceeds two months (GALLARDO, 
1979), drift times te Africa for cards released in the western 
South Atlantic are ~21 months (SHANNON et al., 1973). 
Rafting of several individuals, and possibly involving more 
than one incidence, may account for the occurrences of 
Concholepas on the southwestern African coast. The pos- 
sibility also exists that the species may have temporarily 
colonized the Falklands and mid-Atlantic islands. 

The wide distributions of many Southern Ocean mol- 
lusks is due to the effectiveness of the circumpolar West 
Wind Drift for dispersal (DELL, 1963; POWELL, 1965; 


The Veliger, Vol. 36, No. 3 


BEU, 1976). In support of the importance of rafting, POWELL 
(1965) noted that species associated with algae are partic- 
ularly well distributed. BEU (1976) suggested that colder 
sea temperatures during glaciations were instrumental in 
prolonging the larval lives of several tonnaceans, enabling 
their Southern Ocean dispersal to New Zealand in Pleis- 
tocene times. The Last Glacial recruitment of Subantarctic 
mollusks to the African shelf, from mid-Atlantic islands 
straddling the Subtropical Convergence, accords with en- 
hanced dispersal opportunities resulting from intensified 
Westerlies. Glacial conditions in the Southern Ocean ap- 
parently enhance dispersal opportunities by increasing the 
probability that chance “sweepstake” events are successful. 
Thus the lack of continental shelf areas extending from 
Africa to high latitudes is compensated to some extent by 
the glacial cooling and intensification of the circulation. 
However, for 7awera the colonization of the southern Af- 
rican shelf has been only a temporary advance in the cir- 
cumpolar traverse of the genus back to its Australasian 
region of origin. 

At the Last Glacial Maximum ~ 18 kyr B.P., cooling 
of 3-5°C is indicated by radiolaria from a core taken off- 
shore in the northern Benguela (RC13-229, Figure 1a) 
(Mor.ey & Hays, 1979). This cooling is ascribed to both 
increased input of cooler waters from the south and in- 
creased upwelling stemming from intensification of the 
circulation (MORLEY & Hays, 1979; EMBLEY & MORLEY, 
1980). However, the presence of the Subantarctic mollusks 
does not corroborate colder palaeotemperatures for the 
inshore glacial Benguela environment. Sea-surface tem- 
peratures off Tristan da Cunha vary from ~ 17°C in sum- 
mer to ~ 13°C in winter, while waters off Gough Island 
are 3-4°C colder (ROSCOE, 1979). Inshore temperatures 
in the Benguela region off northern Namaqualand are thus 
similar to those off Tristan, with more local cooling due 
to upwelling producing temperatures similar to those off 
Gough in winter (9-10°C) (SHANNON, 1985). Upwelling 
in the southern Benguela region is strongly modulated 
(subdued) by the passage of frontal systems embedded in 
the Westerlies south of Africa (SHANNON, 1985), but there 
are no data to examine the possibility of decreased up- 
welling associated with the intensified glacial Westerlies. 
Stable isotope (6'8O, 6'°C) and trace element profiles from 
incremental sampling of Recent and fossil bivalve shells 
have been shown to be a record of shelf temperatures, their 
seasonality, and hydrographic events such as upwelling 
(KRANTZ et al., 1987; KRANTZ, 1990). An inner-shelf, 
shallow-infaunal venerid such as 7awera may be a suitable 
candidate for such studies, with dated and analyzed shells 
providing “snapshots” of the late Quaternary Benguela 
inner-shelf environment. 

The timing of the arrival of the Subantarctic mollusks, 
the latitudinal range successfully colonized along the Af- 
rican coast, and when they became locally extinct, are 
outstanding questions. Evidence for arrival during the re- 
gression leading up to the Last Glacial maximum of sea- 
level fall might not be preserved due to erosion as the 


Recthers 1993 


regression continued and subsequent erosion during the 
deglacial transgression. Indications of the timing of their 
local extinction is beneath the Holocene muds landward 
of the relict sediment terrain, where their disappearance 
from the transgressive sand sheet would indicate their de- 
mise. It is possible that warm-water events approximately 
13 and 10 kyr B.P., evidenced by dated Algoa-Natal mol- 
lusks from the sample area (in preparation), might have 
contributed to their extinction. Another possibility is that 
the oxygen-poor, sulphide-rich benthic environment be- 
neath the modern upwelling regime was unfavorable. One 
may speculate that Concholepas concholepas was also re- 
cruited during glacial times, but persisted during the de- 
glacial transgression, only becoming extinct during high 
Holocene temperatures. However, its shells have yet to be 
found in the sediments relict from the Last Glacial shore- 
line and the deglacial transgression. 


ACKNOWLEDGMENTS 


De Beers Marine (Pty) Limited collected the samples and 
made them available to the writer; the support of their 
geological personnel, particularly M. Mittelmeyer and G. 
Esterhuizen, is gratefully acknowledged. M. Bremner 
(Marine Geoscience Unit, Geological Survey of South Af- 
rica) kindly provided material from off Sylvia Hill. J. 
Taylor, British Museum (Natural History), checked the 
identified material against specimens in the BM(NH). M. 
Pether assisted with the illustrations. The Director and 
Council of the South African Museum are thanked for 
sustaining this research. A. Beu and an anonymous referee 
are thanked for their helpful comments. 


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The Veliger 36(3):285-290 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


The Gastropods in the Streams and Rivers of 


Four Islands (Guadalcanal, Makira, Malaita, and 


New Georgia) in the Solomon Islands 


ALISON HAYNES 


School of Pure and Applied Sciences, University of the South Pacific, P.O. Box 1168, Suva, Fiji 


Abstract. Several streams and rivers on the Solomon Islands of New Georgia, Guadalcanal, Makira, 
and Malaita were surveyed for gastropods in 1987 and 1988. Altogether 33 species of freshwater 
gastropods were collected—22 species from New Georgia, 19 from Guadalcanal, 19 from Makira, and 
16 from Malaita. The rivers with low ion content (conductivity 181 us cm~') on the totally volcanic 
island of New Georgia had as many gastropod species as did those with high ion content (conductivity 
234-374 wS cm~') on the partially limestone islands of Guadalcanal, Makira, and Malaita. All species 
belonged to the prosobranch families Neritidae and Thiaridae. 


INTRODUCTION 


Several collections of freshwater gastropods were made 
from New Guinea and Solomon Islands during the nine- 
teenth century. Most of these collections were examined 
and described by RIECH (1937). STARMUHLNER (1976) 
collected freshwater gastropods from the island of Guadal- 
canal and I (HAYNES, 1990) briefly described my collection 
for New Georgia. 

The Pacific island country of Solomon Islands is com- 
posed of six major island groups. These are Choiseul, Santa 
Isabel, Malaita, New Georgia, Guadalcanal, and Makira 
(San Cristobal) (Figure 1). The islands lie just south of 
the equator and as a result the climate is hot and humid 
throughout the year. 

The major islands are steep and large areas arc still 
covered in forest. As a result many of the rivers and streams 
are not readily accessible even though the islands are easily 
reached by boat or plane. 

Gastropods mentioned in this report were collected from 
two streams on New Georgia in 1987 and from Guadal- 
canal, Makira, and Malaita in 1988. This enabled a com- 
parison of the gastropod fauna of two types of island groups, 
one group overlaid with limestone rock (Guadalcanal, 
Makira, and Malaita), the other (New Georgia) lacking 
a limestone overlay. 


STUDY AREA 


The geographical positions of the four islands investigated 
are shown in Figure 1. 

Geologically, Guadalcanal, Makira, and Malaita are 
similar. All have a basement of upper Mesozoic lavas 
overlain by sedimentary rocks, mainly chalky carbonate 
sediments. The New Georgia group on the other hand is 
composed of upper Miocene to Recent andesitic volcanic 
cones, lagoons, and fringing reefs (HACKMAN, 1973). 

Guadalcanal is the largest island in the Solomon Islands 
with an area of 5336 km? and a maximum height of 2447 
m. It and Malaita are the only islands with any length of 
road. All sampling sites (sites 4-9) on Guadalcanal were 
on the more accessible northern coast (Figure 1). Malaita, 
the second largest island, has an area of 4243 km? and a 
height of 1303 m. Here the streams and rivers visited (sites 
16-21) were in North Malaita, near Auki or on the Atori 
road (Figure 1). Malaita is the most densely populated of 
the four islands. Makira, area 3188 km? and height 1250 
m, is mostly inaccessible by road. Sampling was carried 
out on the north coast (sites 10-15) near Kirikiri, the 
Provincial administrative center (Figure 1). The island of 
New Georgia is part of the Western Province. It is a forest- 
clad island with wide lagoons. Most villages have been 
built on the lagoons. The Puha River (sites 1-2) flows into 


Page 286 


CHOISEUL 


The Veliger, Vol. 36, No. 3 


SANTA ISABEL 


SOLOMON ISLANDS 


uo—_—__ 
40 km 


MALAITA 


. 


GUADALCANAL 


MAKIRA 


Figure 1 


A map of the main Solomon Islands showing the localities of the sampling stations on New Georgia, Guadalcanal, 


Makira, and Malaita. 


the Kaisi end of the Marovo Lagoon and can only be 
reached by boat. The Borora River (site 3) is near the 
abandoned logging town and air strip at Borora (Figure 1). 

Several of the rivers on Guadalcanal and Makira were 
carrying a heavy load of sediment washed from the hill- 
sides, where the forest was being logged. 


MATERIALS AND METHODS 


Sampling took place on New Georgia in July 1987 and 
on Guadalcanal, Makira, and Malaita from 26 August to 
6 September 1988, with the exception of site 9 (IGLARM), 
which was sampled in July 1990 (Figure 1). 

The substratum at each station was searched for gas- 
tropods for at least 30 min. The leaf litter, plants, wood, 
and all surfaces of stones and boulders were inspected and 
the sand and gravel were sieved. The specimens collected 
in this way were killed in magnesium sulphate solution 
and then preserved in 80% ethanol for later identification. 

The substratum, pH, water speed, and temperature were 
noted and water samples were collected at some stations. 
These were analyzed for total ions (conductivity wS cm~') 
and hardness (mg CaCO,/L) by the Institute of Natural 
Resources, University of the South Pacific (Table 1). 


RESULTS 


Altogether 33 species of gastropods were collected from 
the Solomon Islands streams and rivers—22 from New 
Georgia, 19 from Guadalcanal, 19 from Makira, and 16 
from Malaita (Table 1). Collecting difficulties, due to con- 
stant rain and swollen rivers, encountered on Malaita may 
account for the smaller number of species found there. 
All gastropods collected belonged to the families Neriti- 
dae and Thiaridae. Voucher specimens of the species col- 
lected were deposited in the Australian Museum, Sydney, 
Australia, and duplicate specimens are available at the 
School of Pure and Applied Sciences, University of the 
South Pacific, Suva, Fiji. The 22 species of Neritidae found 
were Clithon adumorata (Reeve) (C172785), Clithon chlo- 
rostoma (Sowerby) (C172786), Clithon corona (Linné) 
(C172787), Clithon nucleolus (Morelet) (C172788), Ch- 
thon olivaceus (Récluz) (C172789), Clithon oualaniensis 
(Lesson) (C172790), Clithon squarrosus (Récluz) 
(C172791), Clithon waigiensis (Lesson) (C172792), Neri- 
tina asperulata Récluz (C172793), Neritina auriculata La- 
marck (C172794), Neritina canalis Sowerby (C172795), 
Neritina macgillivrayt Reeve (C172796), Neritina petiti Rée- 
cluz (C172797), Neritina pulligera (Linné) (C172798), 


A. Haynes, 1993 Page 287 


Table 1 


The physical conditions, results of water analysis, and gastropods present at the sampling stations 
on the islands of New Georgia, Guadalcanal, Makira, and Malaita. 


To- Hard- 
Water Tem- tal ness 
River speed pera- ions (mg 
Sta- River and width Distance Main (cm ture (uS CaCO,/ 
tion map ref. (m) from sea substratum  sec-!) (°C) cm~')  L) pH Gastropods present 
New Georgia 
1 Puha R. 10 10-40 m stones, 10-20 26 _—- — — Clithon chlorostoma, C. corona, C. 
8°11'S, 157°37'E boulders nucleolus, C’. waigiensis, Neritina 
asperulata, N. auriculata, N. cana- 
lis, N. squamipicta, Septaria tesse- 
lata, S. porcellana. 
2 Puha R. 6 1 km boulders, 50-80 25 181 21.5 6.9  Clithon nucleolus, C. squarrosus, C. 
Solel a5 7.23745; rocks waigiensis, Neritina asperulata, N. 
canalis, N. petiti, N. pulligera, N. 
macgulwrayi, N. squamipicta, N. 
variegata, Neritodryas cornea, N. 
subsulcata, Septaria porcellana, S. 
sanguisuga, Melanoides aspirans, 
M. punctata, Thiara cancellata. 
3. + Borora R. 7 50 m stones 20-30 26 —_ — — Clithon nucleolus, Melanoides tuber- 
8°02’S, 157°35'E culata, M. aspirans, M. cancellata, 
Neritina petiti, N. pulligera, N. 
variegata, Septaria porcellana. 
Guadalcanal 
4 Botanical gardens 5 50 m stones, 20-30 28 — = = Clithon oualaniensis, C. nucleolus, C. 
stream boulders squarrosus, Septaria porcellana, 
9923'S, 159°55’E Thiara scabra. 
5 Botanical gardens 8 0.5 km stones 30-40 28 374 176.51 7.5  Melanoides aspirans, M. punctata, 
stream Neritina canalis, N. variegata, 
9°23'S, 159°55’E Thiara scabra, Tarebia granifera. 
6 Botanical gardens 8 1.5 km stones, 30-50 27 —_— — — Balanocochlis glans, Clithon adumo- 
stream boulders rata, Melanoides punctata, Neri- 
922315 lS 925525; tina canalis, N. variegata, Melan- 
oides arthur, Thiara bellicosa, T. 
scabra. 
7 Mamara R. 5 100 m gravel 0-20 29.5 309 135.13 7.05 Clithon corona, C. nucleolus, Neri- 
9°22'S, 159°54’E tina squamipicta, Septaria porcel- 
lana, Tarebia granifera. 
8  Bonehe R. 11,5} 1.5 km stones B0=50m 2 — Clithon adumorata, C. squarrosus, C. 
9921'S, 159°52'E nucleolus, Melanoides tuberculata, 
M. aspirans, M. pallens, Neritina 
squamipicta, Septaria porcellana, 
Tarebia granifera. 
9 ICLARM 6 10-40 m stones, 0-20 27 = — Clithon chlorostoma, C. nucleolus, 
9°22'S, 159°53’'E gravel Melanoides tuberculata, Neritina 
canalis, N. squamipicta, N. varie- 
gata, Thiara granifera, T. belli- 
cosa, Septaria porcellana. 
Makira 
10 ‘Towitara R. 5 10-100 m __ stones 10-30 25 234 103.84 7.7 Clithon nucleolus, Melanoides punc- 
10°27'S, 161°56’E tata, Neritina auriculata, N. asperu- 
lata, N. variegata, Septaria porcel- 
lana, N. violacea. 
11 ~—- Ravo R. 16 1 km stones 20-50 26 — — —  Melanoides pallens, Neritina pulli- 


10°29’S 161°58’E 


gera, N. variegata, Septaria por- 
cellana, Thiara granvera. 


Page 288 The Veliger, Vol. 36, No. 3 
Table 1 
Continued. 
To-  Hard- 
Water Tem- tal ness 
River speed pera- ions (mg 
Sta- River and width Distance Main (cm ture (uS CaCO,/ 
tion map ref. (m) from sea substratum sec~!) (°C) cm7!)  L) pH Gastropods present 
12. Arohane stream 4 500 m stones 20-40 26 — — —  Balanocochlis glans, Clithon adumor- 
10°28’'S, 161°57'E ata, Melanoides pallens, M. pli- 
caria, Neritina canalis, N. pulli- 
gera, N. variegata. 
13. Kirikiri R. 8 500 m basalt and 30-40 26 273 121.18 7.4  Balanocochlis glans, Clithon nucleo- 
10°27’S, 161°55’E limestone lus, C. olivaceus, Melanoides aspi- 
stones rans, M. pallens, M. plicaria, M. 
punctata, Neritina variegata, N. 
pulligera, Septaria porcellana. 
14 Huro R. 8 10-50 m stones 30-40 27 — = — Clithon corona, C. nucleolus, C. wai- 
10°27'S, 161°54’E giensis, Melanoides pallens, M. 
punctata, Neritina pulligera. 
1S Huro R. 10 1.0 km stones 40-50 26 —_ — — Balanocochlis glans, Clithon corona, 
10°27'S, 161°54'E C. nucleolus, C. olivaceus, Melanoi- 
des aspirans, M. pallens, M. 
punctata, M. plicaria, Neritina as- 
perulata, N. pulligera, N. variega- 
ta, Septaria porcellana, N. squami- 
picta. 
Malaita 
16 Kwaibola R. 10 400 m stones, 30-40 27 ee — Clithon nucleolus, C. squarrosus, C. 
8°40'S, 160°42’E limestones waigiensis, Melanordes pallens, 
Neritina auriculata. 
17 Kwaibola R. 12 1.0 km stones, 30-60 26 288 141.89 7.5 Clithon chlorostoma, C. squarrosus, 
8°40'S, 160°42’E limestones Melanoides pallens, Neritina auric- 
ulata. 
18 UraR. 10 1.5 km stones 30-40 26 — — —  Clithon corona, Melanoides pallens, 
8°49'S, 160°44’E M. punctata, Septaria porcellana. 
19 Kwaiofoa R. 15 1.0 km stones (in 50-80 26 — — Melanoides arthuru, Thiara scabra. 
8°42'S, 160°42’E flood) 
20 Banio R. 8 3.0 km stones, 40-50 26 — |, — Clithon adumorata, Melanoides pal- 
8°30'S, 160°41'E gravel, lens, M. tuberculata, Neritina 
limestones macgillivrayi, Tarebia granifera. 
21 Kao R. 5 12 km boulders, 30-80 25 257 129.99 7.7 Melanoides pallens, M. tuberculata, 
8°35'S, 160°46'E limestone, Neritina variegata. 
rocks 


Neritina squamipicta Récluz (C172799), Neritina variegata 
(Lesson) (C172800), Neritina violacea (Gmelin), Nerito- 
dryas cornea (Linné) (C172801), Neritodryas subsulcata 
(Sowerby) (C172802), Septaria porcellana (Linné) 
(C172803), Septaria sanguisuga (Reeve) (C172804), Sep- 
taria tesselata (Lamarck) (C172805). The 11 species of 
Thiaridae were Balanocochlis glans (v. d. Busch) (C172806), 
Melanoides arthuri (Brot) (G172807), Melanoides aspirans 
(Hinds) (C.1/2808), Melanoides pallens (Reeve) (C172809), 
Melanoides plicaria (Born) (C172810), Melanoides punctata 
(Lamarck) (C172811), Melanoides tuberculata (Miller) 
(C172812), Tarebia granifera (Lamarck) (C172813), Thiara 


bellicosa (Hinds) (C172814), Thiara cancellata Roding 
(C172815), and Thiara scabra Miller (C172816). 

Clithon nucleolus, and sometimes C. squarrosus, were very 
abundant from the mouth to about 0.5 km upstream in 
the rivers and streams on Makira and Malaita. The local 
people on Malaita call them Korona and use them as food. 

The species mixture on Guadalcanal, Makira, and Ma- 
laita was similar, but in the steep fast-flowing Puha River 
on New Georgia, Neritina macgillivrayi was the most abun- 
dant species and Septaria sanguisuga and S. tesselata were 
present; these species of Septaria were not found on other 
islands (Table 1). 


A. Haynes, 1993 


Total ions (234-374 wS cm~') and hardness (103.84- 
176.51 mg CaCO,/L) were high in the rivers of the partly 
limestone islands of Guadalcanal, Makira, and Malaita 
compared with total ions (181 «4S cm~') and hardness (21.5 
mg CaCO,/L) in the Puha River on the completely vol- 
canic island of New Georgia (Table 1). However, the total 
ion content of the water did not appear to influence the 
number of gastropod species in a stream. Although no 
quantitative counts were made, observation showed that 
gastropods were more abundant in streams with high ion 
content. The shells of some species (e.g., Melanoides pallens 
and Neritina variegata) in the streams with high calcium 
carbonate concentration were often heavily encrusted with 
limestone. 

Many specimens of the genus Neritodryas were found 
in small temporary runnels. Their empty shells were also 
found in dried-up runnels suggesting that many of them 
died when the water receded. 


DISCUSSION 


Gastropods were very abundant in the rivers on the islands 
of Guadalcanal, Makira, and Malaita with high ion con- 
tent, but species richness was no greater than on the island 
of New Georgia. Melanoides punctata, M. pallens, and Ta- 
rebia granifera were not found on New Georgia; however, 
this was probably not due to differences in water chemistry, 
but because the streams of New Georgia had beds com- 
posed of boulders and rocks rather than of stones. 

Septaria tesselata and S. sanguisuga were found only in 
the Puha River, New Georgia, although S. tessalata has 
been reported from New Guinea and southeastern Asia. 
The distribution of S. sanguisuga is also widespread. It has 
been found on islands as far apart as Ponepe in the north- 
ern Pacific and Samoa and Fiji in the southwestern Pacific 
(HAYNES, 1990). Septaria sanguisuga and Neritina mac- 
gillivray: may be present in the steeper faster streams on 
the southern sides of Guadalcanal and Makira. 

Although only specimens of the families Neritidae and 
Thiaridae were found on this survey, STARMUHLNER (1976) 
collected the opisthobranch Strubellia paradoxa in the Ma- 
tanikau River, Guadalcanal. 

The neritid and thiarid gastropods are generally sup- 
posed to have originated in southeastern Asia, where most 
species present in New Guinea and the Solomon Islands 
are found (RIECH, 1937; STARMUHLNER, 1976). Two spe- 
cies, Neritina pulligera and N. turrita, have been found in 
Pliocene and Pleistocene rocks in east Java (BENTHEM- 
JUTTING, 1956). Another pointer to a southeast Asian 
origin to the Solomon Islands thiarids and neritids is the 
presence of the same species on Indian Ocean islands— 
e.g., N. pulligera and Clithon chlorostoma on Seychelles and 
Comoros (STARMUHLNER, 1983), Thiara scabra, Mela- 
noides tuberculata and N. auriculata on Mauritius 
(STARMUHLNER, 1983), and Clithon corona, N. auriculata, 
N. variegata, T. scabra, N. pulligera, N. squamipicta, Ner- 


Page 289 


itilia rubida, M. tuberculata, M. plicaria and Tarebia granif- 
era on the Andamon Islands (STARMUHLNER, 1984). 

Of the 33 species of gastropods found on the Solomon 
Islands, 20 of them are present on the Fiji islands (HAYNES, 
1985, 1988, 1990). Eight species have been reported from 
the Fiji islands but not from the Solomon Islands. Some 
species found on the Solomon Islands have not been found 
as far south as Fiji but are in New Caledonia—e.g., Sep- 
taria porcellana, Clithon nucleolus, and Neritina asperculata 
(STARMUHLNER, 1970). On the other hand the species S. 
bougainuiller, S. macrocephala, and Physastra nasuta and the 
genus Fluviopupa are found in Fiji and New Caledonia 
but not in the Solomon Islands. Septaria bougainville: and 
S. macrocephala probably evolved in the Fiji-New Cale- 
donia region (HAYNES, 1992) while the genera Physastra 
and Fluviopupa are of Australian origin (PONDER, 1982; 
WALKER, 1984; HAYNEs, 1990). 

The present distribution of neritid and many thiarid 
freshwater gastropods is thought to have occurred by their 
veliger larvae being carried by ocean currents from island 
to island. I have found that Clithon and Neritina veligers 
can survive in seawater if acclimatized in a series of di- 
lutions that they are likely to experience at the mouth of 
rivers (HAYNES, 1990). 

The water speed, and consequently the nature of the 
substratum, and the number of microhabitats are the major 
factors that determine which species and how many species 
will be found at any one site in a river. These factors are 
more important than water chemistry in determining which 
species of gastropods will inhabit a stream. 


ACKNOWLEDGMENTS 


I thank the Research Committee of the University of the 
South Pacific for a grant that made this work possible and 
the Provincial Premiers and Secretaries of Guadalcanal, 
Makira, and Malaita for their courtesy and help, and the 
villagers of Ramata village, New Georgia for their hos- 
pitality and help. 


LITERATURE CITED 


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Haynes, A. 1985. The ecology and local distribution of non- 
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Haynes, A. 1988. The gastropods in the streams and rivers of 
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Haynes, A. 1990. The numbers of freshwater gastropods on 
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nalen des Naturhistorischen Museum in Wien 86(B):145— 
204. 

WALKER, J. C. 1984. Geographical relationships of the bulin- 
iform planorbids of Australia. Pp. 189-197. In: A. Solem & 
A. C. Van Bruggen (eds.), World-wide Snails: Biogeograph- 
ical Studies on Non-marine Mollusca. Brill/Backhuys: Lei- 
den. 


The Veliger 36(3):291-299 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


NOTES, INFORMATION & NEWS 


Ampullariid Phylogeny—Book Review and 
Cladistic Re-analysis 
by 
Rudiger Bieler 
Department of Zoology, Field Museum 
of Natural History, 
Roosevelt Road at Lake Shore Drive, 
Chicago, Illinois 60605, USA 


A monograph of the gastropod family Ampullariidae was 
recently published. It presents revised hypotheses of am- 
pullaroidean phylogeny and also addresses more general 
issues of phylogenetic systematics (the author, for instance, 
introduces a Fitness-Prinzip to polarize character states). 
An in-depth review of this massive German-language work 
seems appropriate. 


BERTHOLD, Thomas. 1991. Vergleichende Anatomie, 
Phylogenie und historische Biogeographie der Ampul- 
lariidae (Mollusca, Gastropoda). Abhandlungen des 
Naturwissenschaftlichen Vereins in Hamburg (NF) 29: 
256 pp., 358 text-figs. Verlag Paul Parey: Hamburg 
and Berlin. ISBN 3-490-15196-8; DM 98.00; exact 
publication date, 12 December 1991 [O. Kraus, editor, 
in litt.]. 


The monograph is arranged in three main parts (anat- 
omy, phylogenetic reconstruction, biogeography); a taxo- 
nomic appendix is added. The extensive first part (pp. 19- 
129) contains very detailed descriptions of the shell, ex- 
ternal morphology, mantle cavity, circulatory system, al- 
imentary tract, and nervous system, as well as a short 
section on locomotion. Anatomical studies, within each 
topic usually arranged by genus, are documented in great 
detail with numerous line drawings (e.g., of buccal mus- 
culature and nervous system), and are supported by light 
photomicrographs of histological sections (e.g., of the pal- 
lial oviduct) and SEM photomicrographs (e.g., of the am- 
pulla [a modified section of the anterior aorta], of sperm 
in testis follicles, and of radulae). 


Taxonomic Scope of the Work 


On the basis of his anatomical studies of 36 species in 6 
genera, the author recognizes as valid genus-group taxa 
in the Ampullariidae: Afropomus Pilsbry & Bequaert, 1927; 
Saulea Gray, 1867; Lanistes Montfort, 1810 (with sub- 
genus Plesiolanistes Berthold, 1991), Pseudoceratodes Wenz, 
1928; Pila Roding, 1798; Asolene d’Orbigny, 1837; Felip- 
ponea Dall, 1919; Pomella Gray, 1847 (with subgenus 
Surinamia Clench, 1933); Marisa Gray, 1824; and Pomacea 
Perry, 1810 (with subgenus Effusa Jousseaume, 1889). 
Several previously recognized ampullariid taxa (Ampul- 


laria, Ampullarius, Ampulloidea, Ceratodes, Conchylium, 
Kwangispira, Leroya, Limnopomus, Meladomus, Pachychi- 
lus, Pachylabra, Pachystoma, Pomus, Prolanistes, Turbini- 
cola) are placed in synonymy. Not all of the accepted genus- 
group taxa are well supported by autapomorphies. Asolene, 
for instance, is characterized as having secondarily gelat- 
inous eggs (a character unknown for some included spe- 
cies), and the only cited autapomorphy for Plesiolanistes is 
the reduction of shell carinae in the west African popu- 
lations of the single species (p. 210). 

The work is not intended to assist identification at the 
species level. A tally of the number of ampullariid species 
(pp. 20-25) gives a total of approximately 120, a few of 
them known from fossils only. The analysis is restricted 
to a subset of these species, 7.e., those for which anatomical 
material was available to the author. Thirty-two nominal 
species are illustrated by shell photographs (figs. 1-33), 
and 36 nominal species are listed in the Material and 
Methods section (pp. 13-36). For Lanistes, all extant spe- 
cies but L. alexandri were studied anatomically, and this 
genus was treated in greater detail. Few references have 
been included after late 1988, and the current discussion 
of the phylogenetic position of Architaenioglossa (Proso- 
branch Phylogeny volume [PONDER, 1988, ed.] and sub- 
sequent papers) is thus not addressed. 


Taxonomic Treatment 


Compared to the excellent anatomical part of this work, 
the taxonomic part has some problems. Some of this is due 
to technicalities (for instance, the repeatedly mentioned 
ampullariid genus ““Limnopoma’” [e.g., p. 23 as “emend.,” 
p. 203, and cladograms in part 2] should read Limnopomus 
Dall, 1904). The discussion of the family name Pilidae (a 
junior synonym of Ampullariidae) is erroneous (p. 245), 
in that the name was not first introduced by Conolly, 1927, 
as stated, but by PRESTON, 1915:96. 

The family is divided into two subfamilies, monotypic 
Afropominae Berthold, 1991 (with only one Recent spe- 
cies, Afropomus balanoides), and Ampullariinae Perry, 1810. 
The latter is divided into monotypic Sauleini Berthold, 
1991, and Ampullariini. Other previously proposed sub- 
units (such as “Lanistinae” of Starobogatov in SITNIKOVA 
& STAROBOGATOV, 1982) remain undiscussed. In addition 
to formally introducing three ICZN-regulated names (the 
two family-group taxa mentioned above and new subgenus 
Plesiolanistes), Berthold introduced names for several groups 
of ampullariid genera (above genus-, below tribe-level). 
The decision to name most clades in the preferred clado- 
gram resulted in five new names that have no formal 
nomenclatural bearing. One name in particular proves to 


Page 292 


be an unfortunate choice. Berthold introduced the new 
name ‘‘Heterostropha” for the clade comprising the genera 
Lanistes and Pseudoceratodes. However, the identical name 
(Heterostropha Fischer, 1885) is already in use for another 
much larger “informal” group of Gastropoda (e.g., GOLI- 
KOV & STAROBOGATOV, 1975; PONDER & WAREN, 1988). 
More importantly, the phenomenon meant by Berthold in 
using the name Heterostropha is, according to established 
definitions, not heterostrophy but hyperstrophy. Heteros- 
trophy is defined as divergent coiling directions of proto- 
and teleoconch, a condition not known in ampullariids (see 
e.g., LANG, 1900:248, fig. 246; Cox, 1960:/111, fig. 67). 


Methodology 


Berthold aims to reconstruct the phylogeny of Ampullar- 
iidae, based on his studies of comparative anatomy and 
“by consistent application of Hennig’s method of Phylo- 
genetic Systematics” (cover text). He stresses the impor- 
tance of integrating data derived from ecology, ontogeny, 
physiology, and biogeography, to “‘do justice to both aspects 
of phylogenesis—that of cladogenesis and anagenesis,” and 
his study attempts “not only to resolve but to explain the 
phylogenesis of Ampullariidae (p. 8; my translation). 

In addition to providing a monograph of the Ampul- 
lariidae, the author addresses a variety of topics in biology 
and philosophy. Some of this occurs in unexpected places; 
for instance, in the section on the ampullariid nervous 
system, he introduces the term ““Symmetricon” (which the 
author suggests to replace “symmetrical counterpart” in 
morphological descriptions). Important issues that should 
have been discussed in more-developed separate manu- 
scripts (or at least sections) are treated superficially. For 
instance, ‘“‘transformed cladism” is mentioned and curtly 
dismissed, but instead of offering constructive discussion, 
the author broadly advises the reader to study the journal 
Evolution (p. 130). Similarly shallow treatment is given to 
“vicariance biogeography” in the introduction to the chap- 
ter of biogeography (pp. 213-214). The cited literature 
base is small; the treatment of adaptation, for instance, is 
largely restricted to the European body of literature (p. 
13h): 

The second part of the monograph, phylogeny recon- 
struction (pp. 129-213), begins with a chapter on meth- 
odology. Here (pp. 131-133), criteria for polarization and 
ordering of character states are evaluated. Berthold dis- 
cusses Okonomie-Prinzip, as suggested by Bock & WaAH- 
LERT (1965) and PETERS & GUTMANN (1971), a poorly 
known concept in the English-language literature. Dis- 
missing energy consumption as a criterion for character 
evaluation, Berthold introduces Fitness-Prinzip. 

According to the author, the Fitness-Prinzip “permits 
the establishment of correlations between adaptational 
processes and relative fitness as a means of character eval- 
uation” (p. 3). “If a character transformation can be ex- 
pected to increase fitness—it will in following generations 
displace, and finally replace, the ‘inferior’ character state” 


The Veliger, Vol. 36, No. 3 


(p. 137, my translation). However, Berthold does not refute 
Ax’s criticism (Ax, 1988:85-87) that adaptational value- 
hypotheses are non-falsifiable. The penguin example (p. 
133), presented to illustrate the reasoning within the Fit- 
ness paradigm, demonstrates that the polarization (of wing 
structure and function in penguins) is actually based upon 
outgroup comparison (flight ability presumed plesiomor- 
phic), with an a posteriori adaptational “‘explanation.” 

The author employs the Fitness-Prinzip for various 
character states in two organ systems, the lung sac (p. 169) 
and the male copulatory organ (p. 181). In both cases, 
character transformation from simple to complex is as- 
sumed. The alleged adaptational parameters (e.g., im- 
proved oxygen acquisition, reduction of sperm loss) are 
not supported by concrete physiological data. The “‘fitness” 
criterion is applied whenever an adaptational hypothesis 
could be developed. In cases where the Fitness-Prinzip 
appears inapplicable and outgroup comparison cannot help 
(e.g., presence of shell ridges), the author lets congruence 
decide among the hand-constructed cladograms. When a 
hypothesis implies too many convergences, he returns to 
parsimony decisions (“multiple convergent reductions .. . 
a much more cumbersome assumption”; p. 161). 

In the second part of the monograph, character states 
are polarized considering ‘“‘adaptive value” (Fitness-Prin- 
zip sensu Berthold) and outgroup relationship. In the sec- 
tion on conchological characters (including periostracum 
and operculum), the genus Lanistes is treated in detail, 
offering three species-level cladograms in which modifi- 
cations of shell form or carination pattern are given “high- 
est priority” (figs. 324-326). Others are based on lung- 
sac characters, alimentary tract, or combinations of several 
character suites. At the family level, several hand-con- 
structed cladograms are based on character subsets, e.g., 
shell characters, external morphology and mantle cavity 
organs, ampulla shape, kidney, and reproductive, alimen- 
tary, and nervous systems. The various diagrams of re- 
lationship (Verwandtschaftsdiagramme; figs. 327-331, 335- 
341, and 343) are considered largely congruent (p. 198). 
After a reassessment of nominal genera (pp. 199-206), a 
“preferred hypothesis of ampullariid relationships, based 
on character evaluation of all characters here discussed” 
(p. 204; my translation) is offered (z.e., an informal con- 
sensus tree of the diagrams presented before). 


Phylogenetic Analysis 


The phylogenetic part of the work culminates in the pre- 
sentation of a cladogram of phylogenetic relationships 
within the Ampullariidae (figs. 348-349), which is stated 
to be supported by 146 autapomorphies (p. 208). The data 
are not presented in a formal data matrix, instead the 
‘“‘autapomorphies” are numbered and described in the text 
(pp. 209-212). One problem with this approach is that 
the character state distributions in the analysis cannot al- 
ways be unequivocally reconstructed. Since the author of- 
ten describes trends (“secondarily heightened, overall still 


Notes, Information & News 


flat,” “reduced,” “narrowed’’) rather than actual states, 
much information remains subject to interpretation. 

The 146 entries in this list are the total of all character 
state changes, including reversals and parallelisms. Coding 
is inconsistent; for instance, the (congruent) character state 
changes “calcareous egg shell” (#84) and “egg deposition 
outside water” (#85) are coded separately, while the re- 
versals (“eggs secondarily gelatinous and subaquatic” are 
treated as one change (#120, and also #134). The figure 
caption to fig. 348 indicates that there are 11 occurrences 
of convergence in this tree. The text shows there are several 
more (e.g., “median carina reduced,” indicated as conver- 
gence for changes #33 and #77 only, also occurs as changes 
#65 and #75). 

Of the 146 listed character state changes, 80 are syna- 
pomorphies at the family level or autapomorphies of the 
terminal taxa, and thus can only be informative for ingroup 
relationships if they are parts of multi-state character se- 
ries. There is no formal distinction between binary and 
multi-state characters, but some of the listed changes are 
clearly multi-state series (e.g., shell spire shortened [#104], 
further shortened [#107], extremely shortened [#111]). 
With no formal data matrix at hand, interpreting Bert- 
hold’s character state descriptions is sometimes difficult, 
especially since the wording is inconsistent and differs 
between parts of the monograph. In table 1 (conchological 
characters; p. 26), for instance, “inflated” (aufgeblaht) is 
the only term for apertural inflation, while the cladogram 
(fig. 348, pp. 209-212) distinguishes between the states 
“ventrally weakly inflated” (#109), “strongly inflated” 
(#110) and “extremely inflated” (#116). According to the 
list of convergences (fig. 348, caption), the character states 
given for ampulla shape, “secondarily depressed” (#70), 
“secondarily depressed, cigar-shaped” (#133) and “de- 
pressed” (#146), refer to identical character states. Based 
on the same source, “spire and visceral hump flattened” 
(#143), “shell planorboid”’ (#62) and “‘shell and visceral 
hump planorboid” (#127) are also identical. Additional 
complication is caused by use of the term “reduced” (re- 
duziert) instead of presence/absence character states; “‘re- 
duced” seems to indicate “‘lost”’ in some cases, “‘reduced in 
size” in others. 

It is not always clear how character states were scored. 
A certain state used in the analysis for a given taxon 
apparently does not necessarily mean that this state is 
characteristic for all species included. For instance, table 
1 (shell characters) gives up to three possible conditions 
per genus for a character, but only one such condition is 
selected to construct the “preferred tree.”” Another example 
is character state change #145, which marks Pomacea (Ef- 
fusa) as having a flattened pericardium, but the text (p. 
41) mentions an intermediate condition within that group. 

Because no formal data matrix is presented in the work 
and the various trees are constructed by hand, a rigorous 
cladistic analysis based on the presented data seems ap- 
propriate here. This will provide a formal data matrix as 
well as an English-language character listing and descrip- 


Page 293 


tion. The reanalysis is thus not based on new or different 
data, but interprets the available information in a repro- 
ducible fashion to address the following main questions: 
Can a resolved most-parsimonious cladogram be con- 
structed from the published character set? If so, how dif- 
ferent is it from Berthold’s “preferred” version? The most 
interesting point in this reanalysis certainly lies in whether 
a ““most-parsimonious” cladogram without a priori order- 
ing of character states and without weighting differs from 
one that follows Berthold’s “fitness” ordering through ad- 
aptational analyses. 

I have attempted to reconstruct a formal data matrix 
(this Figure 4) from the information in text and figures. 
Because the author did not number characters or character 
states, but assigned numbers to each character state change, 
I could not employ his numbering system. In the following, 
the new numbers assigned for this re-analysis are not 
preceded by “#” to distinguish them from Berthold’s orig- 
inal usage. I included the characters that are synapomor- 
phies at the family level (characters 0-22) to demonstrate 
the ampullariid characters as defined by Berthold; it is 
clear, however, that these do not provide any resolution of 
ingroup relationships. Omitted from the analysis, because 
uninformative in this context, are binary characters defin- 
ing only terminal branches (?.e., autapomorphies of the 
genus-group taxa). The remaining characters were coded 
as binary or (if unequivocal) as multi-state characters as 
given below. In case of ambiguous statements within the 
monograph, information was taken from the descriptions 
on pp. 209-212 and from the list of convergences in figure 
caption 348. The outgroup state was inferred as the state 
opposite to the first change listed in Berthold’s cladogram 
(the author did not employ any particular taxon as out- 
group; Viviparidae are mentioned as one possible sister 
group, and a variety of caenogastropods are used in in- 
formal outgroup comparisons). I have made one exception 
from this procedure; for the fossil genus Pseudoceratodes, 
I have coded all non-shell characters as “unknown.” The 
resulting list comprises 55 binary characters and 15 multi- 
state characters, totalling 161 character states. 

It is important to stress that this is a reconstructed data 
matrix, because the cells in this matrix show the states 
Berthold implied for individual taxa (by placing character 
state changes on branches leading to these taxa), and not 
necessarily always the current state of knowledge for the 
particular taxon. An example is character state change 
#101, which infers a proximal penial sheath gland for, 
among others, Pomella. Berthold (p. 184) cites Hylton- 
Scott (1943; who claimed absence of this structure in Po- 
mella), but assumes that a penial sheath would be found 
if the group were studied histologically. 

Anatomical features, such as alimentary tract and ner- 
vous system, are extensively treated in this work, and it is 
interesting what characters are deemed informative for a 
family-wide phylogenetic analysis. Shell features account 
for 27% (31 states) of the informative characters (7.e., those 
that influence tree topology), although some of these are 


Page 294 


oO : : (7 
PS ae Oe 
a ge gs oF 9 go gd” 


The Veliger, Vol. 36, No. 3 


Explanation of Figures 1 to 3 


Figure 1. Berthold’s preferred hypothesis of phylogenetic rela- 
tionships within the Ampullariidae, based on his figure 348. 


Figure 2. Cladogram derived from data matrix given in Figure 
4. All characters sequentially ordered and given equal weight. | 
= 244, ci = 87, ri = 78; with ingroup symplesiomorphies (char- 
acters 0 to 22) omitted: | = 221, ci = 85, ri = 78; one step shorter 
with characters 30 to 32 coded as 1 instead of O for Plesiolanistes. 


Figure 3. Nelson consensus tree of three equally parsimonious 
cladograms derived from data matrix given in Figure 4. All 
characters unordered and given equal weight. | = 128, ci = 85, 
ri = 83; with ingroup symplesiomorphies (characters 0 to 22) 
omitted: | = 105, ci = 81, ri = 83; one step shorter with characters 
30 to 32 coded as 1 instead of O for Plesiolanistes. Characters 46, 
59, 60, 63 and 65 with retention index <50. 


Notes, Information & News Page 295 
0 1 2 3 4 5 6 i 
01234567890123456789012345678901234567890123456789012345678901234567890 

outgroup 000000000000000000000000000000000000-00- -0000-00----------- 000000- 00000 
Af ropomus 11111111111111111111111010001011001100000000000000000000000100000011010 
Saulea 11111111111111111111111010001000000110001000001000000100000100000022010 
Pseudoceratodes 12727272722222222222222221111010110222222222222227222272222722222722222222227 
Plesiolanistes 111111111111111111111111111010///00120000111001110110210000000000012011 
Lanistes 11111111111111111111111111101001100120000111001110110210000000000012011 
Pila 11111111111111111111111010001011000121111001101010131211000000000012111 
Pomella 11111111111111111111111220032311021121111001111021121311101100000012101 
Surinamia 11111111111111111111111220032211021121111001111021121311101100000012101 
Felipponea 11111111111111111111111220022111010121111001111021121311101100000012111 
Asolene 11111111111111111111111220012011000121111001111021121311101100000012011 
Marisa 11111111111111111111111110103011000031110111111021121311112101101012011 
Pomacea 11111111111111111111111010001011000133111001111021121311112111112112111 
Effusa 11111111111111111111111110001011000032110011111021121311112111112112111 
Figure 4 
Data matrix. “?” character state unknown (fossil group), “—” character state not applicable (character not present), 


“*/? character state either O or 1. 


considered by the author “not a valuable character to re- 
construct phylogenetic relationships” (p. 142, my trans- 
lation). Characters of the female reproductive system, else- 
where in the work described as prone to modifications and 
convergences (p. 189), account for 20% (20 states). Mis- 
cellaneous non-reproductive anatomical characters (25%, 
29 states) and male reproductive characters (24%, 28 states) 
form most of the rest. Data derived from ecology, physi- 
ology, and biogeography (as stressed at the onset, p. 8) are 
hardly realized in the analysis, with only characters 69 
and 70, totalling 4 states. 


The Analysis 


Using the data matrix (Figure 4) the following cladistic 
analyses were performed, employing the computer pro- 
gram Hennig86 (FARRIS, 1988) on a 486-class personal 
computer. The “implicit enumeration” algorithm, guar- 
anteeing to find all equally parsimonious trees, was used. 

(A) All characters were sequentially ordered according 
to the sequence implied by Berthold and given equal weight. 
Two separate runs were made, with characters 30-32 
coded for Plesiolanistes either as 0 or 1 (the character being 
variable between populations of the single species includ- 
ed). Subsequent runs deactivated characters 0 to 22 (the 
in-group plesiomorphies) to attain meaningful numbers 
on tree length (1), consistency index (ci), and retention 
index (ri). 

(B) The same scenario was repeated, with all characters 
unordered. 

The first (ordered) approach resulted in a single most- 
parsimonious cladogram (Figure 2). The subclade orga- 
nization is very similar to Berthold’s preferred tree (Figure 
1) and includes a presumed monophyletic group Pomacea 
+ Effusa, but the overall tree topology is almost inverted, 
with the Marisa-Pomacea-Effusa clade at the bottom. It 


appears that Berthold’s suggested character state ordering 
does not support his overall hypothesis of ampullariid phy- 
logenetic relationships. 

The second (unordered) approach resulted in three 
equally parsimonious trees. The consensus tree (Figure 3) 
is very similar to Berthold’s preferred tree (Figure 1). 
There are only three differences. Afropomus and Saulea 
traded places in the lower part of the tree. Two of the 
three resulting trees resolved Felipponea and Asolene as in 
Berthold’s tree, while the third placed them as a sister 
clade to Pomella + Surinamia. The third difference is that 
the parsimony analysis placed Marisa, not Pomacea, as 
sister taxon to Effusa. The relative position of the subclades 
is obviously very sensitive to ordering of the multistate 
characters in the data set. The parsimony analysis resulted 
in a tree topology almost identical to the one proposed by 
Berthold, without having to resort to character state or- 
dering or character weighting. 


Biogeography 


In the third section of the monograph, the author offers 
seven different scenarios to account for the current distri- 
bution of ampullariid taxa. Ecological and historical (z.e., 
tectonic) parameters are discussed in detail. As a result of 
his biogeographical analyses, Berthold postulates an orig- 
inal Gondwana distribution for the family and states that 
the oldest ampullariid fossils are from Pila in the Eocene 
of Egypt and Kenya. However, this hypothesis is contra- 
dicted by the much older records for Reesidella from the 
uppermost Jurassic and lower Cretaceous of North Amer- 
ica and China. This latter group, presumed to be similar 
to Pila in shell and opercular characters (TOZER, 1956; 
WANG HUuI-JI1, 1984), remains undiscussed. 

In summary, while I disagree with Berthold’s meth- 
odology of arranging intuitively weighted “evolutionarily 


Page 296 


significant” character states into preferred cladograms, it 
should be noted that such a critical estimate of the author’s 
phylogenetic analysis is only made possible by the extensive 
documention of characters in this work. Despite the above 
points of critique, there is no question that Berthold’s 
monograph contains a wealth of information on the family 
Ampullariidae. This work, with its detailed anatomical 
descriptions, will become “required reading” for anyone 
interested in the family. 


Literature Cited 


Ax, P. 1988. Systematik in der Biologie. Darstellung der stam- 
mesgeschichtlichen Ordnung in der lebenden Natur. UTB 
Uni-Taschenbticher 1502, Gustav Fischer: Stuttgart. ix + 
181 pp. 

Bock, W. J. & G. VON WAHLERT. 1965. Adaptation and the 
form-function complex. Evolution 19(3):269-299. 

Cox, L. R. 1960. Gastropoda: general characteristics of Gas- 
tropoda. Pp. /84-/169. In: R. C. Moore (ed.), Treatise on 
Invertebrate Paleontology, Part I, Mollusca 1. Geological 
Society of America and University of Kansas Press. 

Da, W. H. 1904. Notes on the genus Ampullaria. The Jour- 
nal of Conchology 11(2):50-55. 

Farris, J. S. 1988. Hennig86 Reference. Version 1.5 (18 pp. 
manual distributed with program diskette). 

Go.ikov, A. N. & Y. I. STAROBOGATOV. 1975. Systematics of 
prosobranch gastropods. Malacologia 15(1):185-232. 

LANG, A. 1900. Lehrbuch der vergleichenden Anatomie der 
wirbellosen Thiere. Zweite umgearbeitete Auflage. Erste 
Lieferung: Mollusca. Bearbeitet von Dr. Karl Hescheler. 
Gustav Fischer: Jena. vii + 509 pp. | 

PETERS, D. S. & W. F. GUTMANN. 1971. Uber die Lesrichtung 
von Merkmals- und Konstruktions-Reihen. Zeitschrift fur 
zoologische Systematik und Evolutionsforschung 9:237-263. 

PONDER, W. F. (ed.). 1988. Prosobranch phylogeny. Proceed- 
ings of a symposium held at the 9th International Malaco- 
logical Congress, Edinburgh, Scotland. Malacological Re- 
view, Supplement 4. 346 pp. 

PONDER, W. F. & A. WAREN. 1988. Classification of the Cae- 
nogastropoda and Heterostropha—a list of the family-group 
names and higher taxa. Malacological Review, Supplement 
4:288-328. 

Preston, H. B. 1915. Mollusca (Freshwater Gastropoda & 
Pelecypoda). Pp. i-xix, 1-244. In: A. E. Shipley (ed.), The 
Fauna of British India, Including Ceylon and Burma. Taylor 
and Francis: London. 

Sitnikova, T. YA. & Ya. I. STAROBOGATOV. 1982. Volume 
and taxonomic status of the group Architaenioglossa (Gas- 
tropoda, Pectinibranchia). Zoologicheskij Zhurnal 61(6):831- 
842 [in Russian]. 

Tozer, E.-T. 1956. Uppermost Cretaceous and Paleocene non- 
marine molluscan faunas. Geological Survey of Canada 
Memoir 280(2521):v + 125 pp. 

WaNG Hul-Ji. 1984. Two Upper Jurassic gastropod opercula 
in China. Acta Palaeontologica Sinica 23(3):369-372, pl. 1. 


Appendix 


Listing of characters and character states as employed in 
cladistic reanalysis, derived (translated and interpreted) 
from Berthold’s tree (fig. 348) and listing (pp. 209-212). 
Numbers in square brackets refer to Berthold’s original 


The Veliger, Vol. 36, No. 3 


” 


“autapomorphies.”” Binary characters defining autapo- 
morphies of terminal taxa omitted. 


Unreversed Synapomorphies at Family Level 
(z.e., only outgroup differs in state) 


(0) shell suture edged: no (0), yes (1 [#2]) 

(1) labial tentacles: not present (0), present (1 [#4]) 

(2) osphradial length: not shortened (0), shortened (1 

[#5]) 

(3) lung sac: not present (0), present (1 [#6]) 

(4) gill moved to right side: no (0), yes (1 [#8]) 

(5) anterior aorta forms ampulla: no (0), yes (1 [#9]) 

(6) anterior kidney chamber: not present (0), present (1 

[#10)]) 

bipartite copulatory organ {penis + penis sheath} on 

right mantle margin: not present (0), present (1 [#11]) 

(8) eupyrene and atypical sperm anchored in nurse cells: 
no (0), yes (1 [#12]) 
(9) spermatophore: present (0), reduced (1 [#13]) 

(10) pallial oviduct with 3 accessory glands: no (0), yes 
(1 (#14) 

(11) jaws: not enlarged (0), enlarged (1 [#18]) 

(12) number of radular rows: not reduced (0), reduced (1 
[#19]) 

(13) radular teeth with few but enlarged cusps: no (0), 
yes (1 [#20]) 

(14) inner marginal radular tooth: without basal lobe (0), 
with basal lobe (1 [#21]) 

(15) number of medio-dorsal protractors of buccal mass: 
not reduced (0), reduced (1 [#22]) 

(16) esophageal pouches with demarcated esophageal 
gland: no (0), yes (1 [#23]) 

(17) two median stomach grooves: not present (0), present 
(1 [#24]) 

(18) intestine elongated and repeatedly coiled: no (0), yes 
(1 [#25]) 

(19) pleurosupraintestinal zygosis: not present (0), pres- 
ent (1 [#26]) 

(20) subintestinal ganglion fused with right pleural gan- 
glion: no (0), yes (1 [#27]) 

(21) pleural commissure: not present (0), present (1 [#28]) 

(22) pedal and pleural ganglia fused on both sides: no (0), 
yes (1 [#29]) 


(7 


wa 


Characters Informative for Ingroup 
Relationships 


Shell characters (outgroup state = 0) 


(23) shell shape: egg-shaped (0), planorboid (1 [#62, #127, 
#143]), weakly neritoid (2 [#103]) 

(24) whorl shape: moderately bulging (0), strongly bulg- 
ing (1 [#1]), flattened (2 [#106]) 

(25) hyperstrophy: no (0), yes (1 [#61]) 

(26) umbilicus: narrow (0), wide (1 [#63, #129]) 

(27) spire: not shortened (0), shortened (1 [#104)), further 
shortened (2 [#107]), extremely shortened (3 [#111]) 


Notes, Information & News 


(28) aperture: round (0), broadly oval (1 [#3]), acutely 
oval (2 [#105]), kidney-shaped (3 [#128)]) 

(29) aperture: small (0), ventrally weakly inflated (1 
[#109]), strongly inflated (2 [#110]), extremely in- 
flated (3 [#116]) 

(30) dorsal carina: present (0), reduced (1 [#32, #64, 
#76, #73-in part}) 

(31) median carina: present (0), reduced (1 [#33, #65, 
#75, #77, #73-in part]) 

(32) umbilical carina: not present (0), present (1 [#66, 
#73-in part]) 

(33) longitudinal striping: present (0), reduced (1 [#108)), 
completely reduced (2 [#112]) 


Non-reproductive anatomical characters 


(34) visceral hump: not shortened (0), shortened (1 [#34, 
#114}) 

(35) mantle cavity: not broadened (0 [#130, #144; as 
“narrowed’’]), broadened (1 [#7]) 

(36) lung sac opening: non-closable (0 [#6]), closable (1 
[#37]), with closing tube (2 [#53]), with prolonged 
closing tube (3 [#121]}) 

(37) ingestion siphon: not elongated (0), elongated (1 
[#78]), further elongated (2 [#137]), extremely elon- 
gated (3 [#142]) 

(38) ingestion siphon forming breathing tube: no (0), yes 
(1 [#79]) 

(39) lung sac pump breathing: no (0), yes (1 [#80]) 

(40) ampulla shape: depressed (0 [#9, #70, #133, #146)), 
enlarged, vertically egg-shaped (1 [#39]) 

(41) auricle-ventricle axis: perpendicular to aorta axis (0), 
tilted toward aorta axis (1 [#132]) 

(42) pericardium: round (0), flattened (1 [#68, #131, 
#145)) 

(43) posterior kidney chamber with lobe: no (0), yes (1 
[#55]) 

(44) central radular tooth: trapezoidal (0), rectangular (1 
[#86]) 

(45) pleuro-supraintestinal zygosis: not broadened (0 
[#26]); broadened (1 [#102]) 

(46) cerebral commissure in cross-section: round (0), flat- 
tened (1 [#43]) 

(47) origin of anterior osphradial nerve moved anteriorly: 
no (0), yes (1 [#72]) 


Reproductive characters, male 
(outgroup state: not applicable’) 


(48) penis length: not prolonged (0 [#11]), prolonged (1 
[#57]), prolonged and coiled in pouch (2 [#98]) 


' These characters are not present in the outgroup, and thus 
no outgroup comparison is possible to infer character polarity in 
this character suite. The bipartite copulatory organ (penis and 
penial sheath), as a derivative of the right mantle margin, is an 
autapomorphy of the Ampullariidae (e.g., the copulatory organ 
in the presumed sistergroup Viviparidae is a modified right ce- 
phalic tentacle). 


Page 297 


(49) penial sperm groove: open (0), closed to form central 
channel (1 [#99]) 

(50) penial sheath length: not prolonged (0 [#11]); pro- 
longed (1 [#56]) 

(51) distal penial sheath gland: not present (0); epithelial 
cells at distal inner margin of penial sheath prolonged 
(1 [#59]); present, weak (2 [#82; 7.e., further elon- 
gation of cells, see p. 180]), epithelial cells extremely 
prolonged (3 [#91]) 

(52) outer penial sheath gland: not present (0), present (1 
[#83]) 

(53) penial bulb: not present (0); present (1 [#40]), en- 
larged (2 [#58]), widened into penial pouch (3 [#97]) 

(54) epithelium at base of copulatory organ in grooves: no 
(0), yes (1 [#60]) 

(55) copulatory organ with sperm groove lobe: no (0), yes 
(1 [#81)) 

(56) distal penial sheath gland enlarged by subepithelial 
glands: no (0), yes (1 [#100]) 

(57) distal penial sheath gland with basal lobe: no (0), yes 
(1 [#123]) 

(58) proximal penial sheath gland: not present (0); pres- 
ent, weak (1 [#101]); enlarged (2 [#122]) 


Reproductive characters, female 


(59) receptaculum seminis with separate exit duct: yes (0 
[#71, #93]), no (1 [#16]) 

(60) receptaculum seminis moved proximally toward coiled 
oviduct: no (0), yes (1 [#140]) 

(61) pallial oviduct with numerous lateral pouches: no (0), 
yes (1 [#126]) 

(62) shell gland with diverticle: no (0), yes (1 [#124]) 

(63) shell gland coiled into primary and secondary helices: 
no (0), yes (1 [#138]) 

(64) pseudo-bursa formed by atrium of receptaculum sem- 
inis: no (0), yes (1 [#125]); yes, separated from re- 
ceptaculum by tube-shaped section of pallial oviduct 
(2 [#141]) 

(65) size of proximal albumen gland: not reduced (0 [#14]); 
reduced (1 [#139; 7.e., small parts present, see p. 
184]) 

(66) pallial oviduct with albumen gland diverticles: no (0), 
yes (1 [#15]), reduced (2 [#49]}) 

(67) bursa copulatrix: normal (0), enlarged (1 [#36]), 
reduced (2 [#41]) 

(68) calcareous egg shell (= egg deposition outside water): 
no (0 (#120, #134]), yes (1 [#84, #85)]) 


Other characters 


(69) diet: microphagous (0 [#113]), macrophagous (1 
[#17]) 

(70) sinking behavior with extended foot: no (QO), yes (1 
[#54]) 


Page 298 


Questionable Species in the 
Cephalopod Genus Argonauta 
by 
Kent D. ‘Trego 
3895 LaSelva Dr., Palo Alto, California 94306, USA 


HOcHBERG et al. (1992) list six species of living Argonauta 
in their discussion concerning larval forms of this genus: 
A. argo (Linnaeus, 1758), A. nodosa (Lightfoot, 1786), A. 
hians (Lightfoot, 1786), A. noury: (Lorois, 1852), A. boett- 
geri (Maltzan, 1881), and A. cornuta (Conrad, 1854). Of 
these six species, A. boettgerx and A. cornuta should be 
considered questionable. 

The shell of Argonauta boettgeri (Figure 1A—C), which 
is very rare, is similar in appearance to that of A. hzans 
(Figure 1D-F). On the basis of female arm length (NEsIs, 
1987), no distinction is made between A. boettgeri and A. 
hians, and ROBSON (1932) considers the possibility that A. 
boettgeri is a form of A. hians. 

Argonauta cornuta has the same eastern Pacific range as 
A. nouryi and the differences between the shells of A. cor- 
nuta and A. noury: reflect the variation pattern seen in A. 
hians (Figure 1G-K). What distinguishes the shell of A. 
cornuta from that of A. nouryz is the presence of what have 


The Veliger, Vol. 36, No. 3 


been termed “flutes” or “horns” on the shell aperture. The 
shell of A. hians may or may not have flutes or horns on 
the aperture. To a much lesser degree, flute or horn struc- 
tures may be present on the shells of A. argo and A. nodosa. 

Until further quantitative work is done on the shell and 
soft parts of Argonauta boettgeri and A. cornuta, these species 
remain questionable. Specimens of A. boetigeri, A. cornuta, 
and A. noury: are included in the collection of the California 
Academy of Sciences, although these specimens have not 
yet been assigned identification numbers. 


Literature Cited 


HOcHBERG, F. G., M. Nixon & R. B. Touu. 1992. Order 
Octopoda Leach, 1818. Pp. 213-279. In: M. J. Sweeney, C. 
F. E. Roper, K. M. Mangold, M. R. Clarke & S. V. Boletzky 
(eds.), “Larval” and Juvenile Cephalopods: A Manual for 
Their Identification. Smithsonian Contributions to Zoology, 
No. 513, Smithsonian Institution Press: Washington, D.C. 

NEsis, K. N. 1987. Cephalopods of the World: Squids, Cut- 
tlefishes, Octopuses, and Allies. T. F. H. Publications: Nep- 
tune City, New Jersey. 351 pp. 

Rosson, G. C. 1932. A monograph of the recent Cephalopoda, 
Part 2: The Octopoda, excluding the Octopodinae. Vol. 2. 
359 pp. 


Notes, Information & News Page 299 


K 


J 


Figure 1 


A. Argonauta boettgeri (45 mm). B. A. boetigeri (32 mm) at left and A. boettgeri (33 mm) at right. C. A. boettgeri 
(47 mm). D-F. A. hians (54 mm, 47 mm, 52 mm). G. A. cornuta (71 mm) aperture view. H. A. noury: (66 mm) 
aperture view. I. A. noury: (76 mm) aperture view showing characteristics of both A. noury: and A. cornuta. J, K. 
A. hians (92 mm, 86 mm) variations, aperture view. 


The Veliger 36(3):300-302 (July 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


BOOKS, PERIODICALS & PAMPHLETS 


Pacific Coast Nudibranchs, Second Edition 


by Davip W. BEHRENS. 1991. Sea Challengers, 4 Somerset 
Rise, Monterey, CA 93940. vi + 107 pp. Price: $25.95 
(US.). 


On a recent expedition to the Gulf of California, I had 
collected an anomalous specimen of Acanthodoris which I 
could not immediately identify. After returning to town, I 
photographed the animal under the dimming light of a 
January late-afternoon cloud cover. All that day, the elec- 
tric generator for the whole town of Bahia de los Angeles 
had not been working because their diesel supply had run 
out. Sitting in my hotel room after sunset, by the quivering 
yellow light of an oil lantern, I determined the species of 
my unidentified animal using David W. Behrens’ second 
edition of Pacific Coast Nudibranchs. This book works un- 
der Baja California field-tested conditions! It is scientifi- 
cally accurate, clearly understandable, and communicates 
a wealth of information. The descriptions are clear, in- 
formative, and relate to living creatures one will find in 
eastern Pacific intertidal and subtidal regions from Alaska 
to the tip of Baja California. 

Pacific Coast Nudibranchs is a field guide with three main 
sections: introductory material, species descriptions (the 
heart of the book), and a classification scheme and liter- 
ature cited. 

The first section is 28 pages of well-written and useful 
text summarizing what we know about the biology and 
anatomy of the Opisthobranchia. It describes their general 
characteristics and evolutionary adaptations (emphasizing 
their shift from using a protective shell to chemical defen- 
sive means). Behrens then presents terse, clear summaries 
of feeding and the radula, sensory organs and the rhino- 
phores, respiratory appendages, and opisthobranch repro- 
duction. Each topic is superbly illustrated. 

The introductory section concludes with a pictorial glos- 
sary and dichotomous key to the opisthobranch orders and 
suborders. The line drawings and key will lead anyone 
(even someone unfamiliar with the curious anatomical 
structures of sea slugs) to the correct section of the color 
photographs of species to identify his or her “slug at hand.” 

The species descriptions (pages 28-100) include full 
color photographs of 217 species of opisthobranchs with 
descriptive notes. For every species, there is a verbal de- 
scription of the salient external diagnostic features, a rad- 
ular formula, size, range, and natural history notes. Nu- 
merous references document the sources of the information. 
I found relatively few errors in the text (Elliot, on pages 
80 and 102, being the most obvious, misspelling a famous 
author’s name). 

Of special note, the author and year citation is given for 
each species. Some species have their common English 


names listed in small print, but many do not; the emphasis 
is properly on the correct scientific name of the species. 

Most of the photographs are excellent, depicting the 
colors and shapes of these foudroyantly beautiful ocean 
dwellers. Even casually paging through the book, one fre- 
quently pauses on a photograph because of the brilliance 
of its color, the sharpness of the image, or the marvelous 
morphological diversity of the organism. Many are obvi- 
ously aquarium-staged photographs; the best are in situ 
photographs that reveal the biology of the species (e.g., 
Phyllaplysia taylor: Dall, 1900, on the seagrass Zostera, and 
Elysia hedgpethi Marcus, 1961, on the finger alga Codium). 
Photographing these incredibly colorful organisms, often 
only 5-25 mm in length, is extremely difficult. Dave Beh- 
rens is to be complimented on assembling richly useful 
photos of all the species he discusses. The combination of 
introductory keys, descriptions of salient anatomical fea- 
tures, and the excellent photographs almost guarantees the 
user’s ability to identify any Pacific coast opisthobranch. 

Concluding the guidebook are a classification scheme of 
the opisthobranch mollusks described in the book, and 
three pages of literature cited. The majority of the refer- 
ences were published since 1980 (after the publication of 
the first edition). This extremely valuable section allows 
nearly an immediate entrance into the incredibly large 
number of opisthobranch publications that have appeared 
in the last decade. 

An index to scientific names (thankfully omitting an 
index to English common names) is on the inside cover 
and endpage. I think that the addition of another folio of 
pages (or even half-folio) would have given the author 
extra pages to spread out a few tight layouts, add some 
historical information, and include several maps. 

One must contrast this new edition with Dave’s first 
edition. The layout of the species descriptions is different; 
the photograph and description are on the same page, with 
illustrations therefore appearing on the outer half of each 
page, rather than text on one page and illustrations on the 
facing page. This welcome change makes the book far more 
useful, because one can cursorily thumb through the book 
to find an animal, without having to open and search the 
“innards” of every page. Species coverage, quality of pho- 
tographs, and bibliography are bigger and better than the 
first edition. 

Comparing the two editions, published 10 years apart, 
documents the progress that has been made in our knowl- 
edge and understanding of alpha-level (and higher) tax- 
onomy, evolutionary ecology, and the zoogeography of the 
opisthobranch gastropods in the eastern north Pacific tem- 
perate and cold water faunal regions. The first edition of 
Dave’s Pacific Coast Nudibranchs played an instrumental 
role in stimulating and encouraging a significant amount 


Books, Periodicals & Pamphlets 


Page 301 


of this new research. I believe his second edition will be 
equally pivotal. 


Hans Bertsch 


Pacific Coast Nudibranchs: 
Supplement I. Radula 


by Davip W. BEHRENS. 1992. Sea Challengers, 4 Somerset 
Rise, Monterey, CA 93940. 11 pp., 150 illus. Price: $6.95 
(shipping and handling $1.80). 


This booklet is a necessary supplement to Dave Behrens’ 
Pacific Coast Nudibranchs, second edition (1991). In it are 
assembled line drawings of the radular teeth of 150 opis- 
thobranch species that occur on the American Pacific coast 
from Alaska to Baja California. The cover is a beautiful 
scanning electron micrograph of the radula of the hydroid- 
feeding eolid nudibranch Bajaeolis bertschi. 

The introduction is a tersely written summary of the 
taxonomic uses of radulae (citing my paper on ontogenetic 
and intraspecific variation of opisthobranch radulae), their 
overall structure and function, and how to extract and 
mount a radula for study (referring to Tom Thompson’s 
method), and it includes references for the major sources 
of the included drawings (MacFarland and McDonald). 

When I received this booklet, I spent a lot of time pe- 
rusing the drawings, thinking about the different shapes, 
the species’ prey items, and reasons for differences and 
similarities. For instance, the sponge-feeding notaspidean 
Anidolyta spongotheras has radular teeth similar to those 
of the sponge-feeding nudibranch species of Cadlina and 
other chromodorids, yet is distinctly different from the 
sponge-feeding teeth of species of Aldisa. 

This publication highlights the diversity of opistho- 
branch feeding structures and should encourage much 
thought and study about their functional morphology. It 
is highly recommended. 


Hans Bertsch 


The Genus Chicoreus and Related Genera 
(Gastropoda: Muricidae) in the Indo-West Pacific 


by ROLAND HouartT. 1992. Memoires du Museum Na- 
tional d’Histoire Naturelle, Zoologie, tome (A) 154. 188 
pp., 480 figures, 4 tables. Price: Dfl 125.00 (about US$ 
74.00) plus postage. 


Species of the muricid genus Chicoreus Montfort are 
arguably the most beautiful of the family. Certainly they 
are the most numerous in numbers of species (about 90 
world-wide). And, as they frequently occur in shallow 


water or even intertidal environments, they are well-rep- 
resented in most collections. They are also the most com- 
plex of the groups in the Muricinae, as a result of a more 
than usual amount of intraspecific variation. 

Because of the ready availability of specimens, from the 
time of Linnaeus numerous species have been erected— 
most without much more than an oftimes poor illustration 
in an iconography (e.g., Martini and Chemnitz) to serve 
as a type, or an even worse original illustration in the case 
of Perry. With the advent of workers such as Sowerby and 
Reeve, and Kiener for the species of Lamarck, the illus- 
trations improved considerably and in many cases, though 
by no means all, there is actually a specimen somewhere 
upon which the illustration was based. If this model can 
be located then it is an invaluable type specimen. 

Just to give an idea of the magnitude of the problem, 
Houart has accepted a total of 64 Recent taxa in the three 
genera he is monographing (Chicoreus, Chicomurex, and 
Naquetia) but these 64 species have a total of 77 synonyms 
between them. If one excludes the 16, mostly deep-water 
forms that have been named since 1980, the numbers are 
even more daunting: 48 species with 77 synonyms. One 
well-known species, Chicoreus brunneus (Link), alone has 
10 synonyms. 

To clean up this clutter of taxa is a job second only to 
the Aegean stables—but Houart has attacked it with the 
vigor of Hercules and even though I am not 100% satisfied, 
certainly I can accept the results. It is my personal feeling 
that it is better for me to decide that this is the final word 
and let the malacological community re-label their collec- 
tions one last time than to persist in any disagreement over 
subjective synonyms. 

To establish these synonymies Houart has done an 
amazing job of locating type material and especially of 
figuring these obscure types. Of the over 400 illustrations 
of specimens, one-third represent type material. This alone 
makes the book worth its somewhat hefty price. But even 
more than that, the illustrations are uniformly well done, 
and the four plates of color illustrations are especially 
gorgeous. 

In the systematics there will not be too many changes 
to cause pain to the collector. Only one “familiar”’ species 
has disappeared, that being Chicoreus penchinati (Crosse), 
which has disappeared into the synonymy of C. strigatus 
(Reeve). Species of what heretofore have been considered 
to be Chicoreus s.s. are divided into a subgenus Chicoreus 
s.s., characterized by the presence of a labral tooth, and a 
subgenus 7riplex Perry, lacking this tooth. Having par- 
ticipated in the dismemberment of Murex s.s. on the same 
grounds, I can scarcely find fault with this division. One 
new subgeneric taxon is proposed, Chicopinnatus (type 
species: Pterynotus orchidiflorus Shikama), for those few 
species that have the superficial appearance of the genus 
Pterynotus, with three winged varices, but have the early 
development of Chicoreus. 

The two taxa Naquetia Jousseaume and Chicomurex 
Arakawa, formerly considered to be subgenera of Chico- 


Page 302 


The Veliger, Vol. 36, No. 3 


reus, are elevated to generic level (these are the “related 
genera” of the title) on the basis of their radular mor- 
phology. I wonder if a better arrangement would not be 
to have the genus Naquetia, with subgenera Naquetia s.s. 
and Chicomurex ? 

In addition to the large number of illustrations of spec- 
imens there are also distribution maps for each taxon, and 
of extreme value are the enlarged drawings of protoconchs 
for 55 Recent species (often more than one example) and 
six fossil species. 

The general format of the book and its overall excellent 
quality is a tribute to Philippe Bouchet, of the Museum 
National d’Histoire Naturelle. From an editorial or pro- 
duction perspective it is hard to find fault, but I would 
have liked to see the figure numbers for multiple specimens 
of the same species a little more conspicuous (I have simply 
underlined them in my copy). 

The only serious error that I have encountered is the 
omission of any explanation for figure 302, which is a 
specimen of Chicoreus rubescens (Broderip, 1833) identified 
in a subsequent work (Apex, 1992, Vol. 7, Nos. 3-4, fig. 
4) as a specimen in Houart’s collection—47.8 mm from 
? Tahiti. 

The only other, less serious, error is the plate expla- 
nation for figure 339, which is stated to be a neotype 
(BMNH 1984076) for Chicoreus banks (Sowerby), but 
in the text it is correctly stated to be the lectotype of Murex 
crocatus Reeve. The latter name Houart places in the syn- 
onymy of C. banksi, but here is the one synonymy with 
which I must take issue. Houart has rightly demonstrated 
that C. bourguinati (Poirier) is one name for the East Af- 
rican (Durban to [?] Sri Lanka) species that most workers 
have called C. banksi. He is of the opinion that the Indo- 
West Pacific (Malaysia to new Caledonia) form variously 


referred to C. banksw, C. crocatus, and (totally erroneously) 
C. axicornis (Lamarck) is not the same as the East African 
one. 

Although I am completely willing to accept this division, 
the question becomes what name is to be used for which 
species. He has selected a specimen in the British Museum 
to serve as lectotype of Chicoreus banksi (BMNH 197478), 
which is said to have come from “the Moluccas.” 

This, I believe, is the root of Houart’s mistake. First, 
this large (77.5 mm) shell is not Sowerby’s illustrated 
specimen, which according to the original description (1841, 
Proceedings of the Zoological Society of London, Pt. 8, p. 
140) measures ‘2.8 poll.” [=70.8 mm]. Second, another 
specimen in the British Museum measures 70 mm in height, 
is very like the illustration given by Sowerby (1841, Con- 
chological Illustrations, fig. 82), and can be matched to 
specimens from Zanzibar (e.g., that figured by Vokes, 1978, 
Annals Natal Museum, Vol. 23, pl. 3, fig. 3). 

This latter specimen should have been selected as the 
lectotype of Chicoreus banks; however, it is not too critical 
because the larger shell is clearly also an East African 
specimen. If one compares this “‘lectotype” of C. banksi 
(Houart’s fig. 178) and the lectotype of C. bourguinati 
(Houart’s fig. 261) it is obvious that they are conspecific; 
I can match it also with specimens in my own collection 
from the Seychelles. I assume that the “Moluccas” locality 
is just another example of incorrect data in old collections 
and does not place the species in the western Pacific. 

Therefore, it seems to me that the name Chicoreus banks11 
must be returned to the East African population, with C. 
bourguinati as a synonym. For the Indo-West Pacific pop- 
ulation the name C. crocatus is available. 


Emily H. Vokes 


In Memoriam 
Ralph I. Smith 


For years of steadfast service 
and contributions to C.M.S. 
and invertebrate zoology. 


Information for Contributors 


Manuscripts 

Manuscripts must be typed on white paper, 842” by 11”, and double-spaced throughout 
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review process, manuscripts, including figures, should be submitted in triplicate. The 
first mention in the text of the scientific name of a species should be accompanied by the 
taxonomic authority, including the year, if possible. Underline scientific names and other 
words to be printed in italics. Metric and Celsius units are to be used. 

The sequence of manuscript components should be as follows in most cases: title page, 
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erature cited, figure legends, figures, footnotes, and tables. The title page should be on a 
separate sheet and should include the title, author’s name, and address. The abstract 
should describe in the briefest possible way (normally less than 200 words) the scope, 
main results, and conclusions of the paper. 


Literature cited 

References in the text should be given by the name of the author(s) followed by the 
date of publication: for one author (Smith, 1951), for two authors (Smith & Jones, 1952), 
and for more than two (Smith ef al., 1953). 

The “literature cited” section must include all (but not additional) references quoted 
in the text. References should be listed in alphabetical order and typed on sheets separate 
from the text. Each citation must be complete, with all journal titles unabbreviated, and 
in the following form: 


a) Periodicals 
Cate, J. M. 1962. On the identifications of five Pacific Mitra. The Veliger 4:132-134. 


b) Books 


Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London. 
288 pp. 


c) Composite works 


Beder, HW. M: 1980. Asteroidea: the sea stars. Pp. 117-135. In: R. H. Morris, D. P. 
Abbott & E. C. Haderlie (eds.), Intertidal Invertebrates of California. Stanford Univ. 
Press: Stanford, Calif. 


Tables 
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CONTENTS — Continued 


Studies on the reproduction and gonadal parasites of Fissurella pulchra (Gas- 
tropoda: Prosobranchia) 
MARTA BRETOS*AND RICARDO' Hi: CHIHUAILAB 4230 see eee 245 


Genital dimorphism in the land snail Chondrina avenacea: frequency of aphally 
in natural populations and morph-specific allocation to reproductive or- 
gans 
BRUNO BAUR AND XIAOFENG GHEN (2.00992) 2 We aoe ee ZOD, 


A new species of Otostoma (Gastropoda: Neritidae) from near the Cretaceous/ 
Tertiary boundary at Dip Creek, Lake Nacimiento, California 
RICHARD L. SQUIRES AND) LouELLA ReSAULY 722524. 22 eee 259 


The nautilid Eucymatoceras (Mollusca: Cephalopoda) in the Lower Cretaceous 
of northern California 
PETER U. RoDDA, MICHAEL A. MURPHY, AND CLARENCE SCHUCHMAN ... 265 


Earliest record of the anomiid bivalve Pododesmus: a new species from the lower 
Eocene of western Washington 
RICHARD LsSQUIRES’. 2.40.4 enor Set oe ee eee 270 


Relict shells of Subantarctic Mollusca from the Orange shelf, Benguela region, 
off southwestern Africa 
JOHN:PETHER: 3 f.: 0.653 ets asi es wos epee Gian CEES te See ee 276 


The gastropods in the streams and rivers of four islands (Guadalcanal, Makira, 
Malaita, and New Georgia) in the Solomon Islands 
ATLISON'. FIAYINES 0.2.00 Meee 8 Set tn aes he ae aN et rr 285 


NOTES, INFORMATION & NEWS 


Ampullariid phylogeny—book review and cladistic re-analysis 
RUDIGER BIEGER® 2:..3.)dvjsy0 so Re ek ee ee ee 291 


Questionable species in the cephalopod genus Argonauta 
KENT: Dy PREGGO ss ee Se GRE oe ee Ee te ee ee eee 298 


ISSN 0042-3211 


THE 


VELIGER 


A Quarterly published by 
CALIFORNIA MALACOZOOLOGICAL SOCIET/ 
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R. Stohler, Founding Editor 


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fT 29 1993 


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Volume 36 October 1, 1993 Number 4 


CONTENTS 


Local and regional abundance patterns of the Ascoglossan (= Sacoglossan) opis- 
thobranch Alderia modesta (Lovén, 1844) in the northeastern Pacific 
CVNGETAMD) MERROW BRIDGE ities sae She been ae neve Rien G 303 


The influence of olfactory and tactile stimuli on the feeding behavior of Melibe 
leonina (Gould, 1852) (Opisthobranchia: Dendronotacea) 
WINSOR H. WATSON III AND CHARLES M. CHESTER .................-. 311 


Ecological, morphological, and genetic differences between the sympatric bivalves 
Donax variabilis Say, 1822, and Donax parvula Philippi, 1849 
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Larval morphology of the scallop Argopecten purpuratus as revealed by scanning 
electron microscopy 
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THE VELIGER 
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Local and Regional Abundance Patterns of the 


Ascoglossan (= Sacoglossan) Opisthobranch 
Alderia modesta (Loven, 1844) in the 


Northeastern Pacific 


by 


CYNTHIA D. TROWBRIDGE! 


Department of Biology, Syracuse University, Syracuse, New York 13244, USA 


Abstract. 


The ascoglossan (= sacoglossan) opisthobranch Alderia modesta (Loven, 1844) associates 


with the high intertidal, mat-forming, yellow-green alga Vaucheria (Chrysophyta: Xanthophyceae) in 
temperate estuaries throughout much of the Northern Hemisphere. Although A. modesta has been 
extensively studied on N.E. and N.W. Atlantic shores, complementary information for N.E. Pacific 
estuaries is sparse. The opisthobranch was common on Vaucheria mats in Yaquina Bay and Coos Bay, 
Oregon, USA with mean densities ranging from tens to hundreds per square meter of algal mat. In 
Oregon, A. modesta was present throughout the entire year. During winter, the ascoglossan persisted 
on Vaucheria within gaps of salt marsh vegetation and in sunny microhabitats with a southern exposure. 
The opisthobranch numerically dominated the epifaunal invertebrate assemblage associated with Vauche- 
ria mats. In northern California, USA, A. modesta was sparse in Humboldt Bay and apparently absent 
from Arcata Bay and Eel River Slough. The species was patchily distributed within Bodega, Tomales, 
and Drakes bays in California with mean densities <20/m’. High densities of predators, particularly 
shorebirds and the mud-flat crab Hemigrapsus oregonensis, may reduce ascoglossan densities in California 


though other factors may contribute as well. 


INTRODUCTION 


Estuaries are complex ecosystems composed of several bi- 
ologically important intertidal habitats including salt 
marshes, mud flats, and eelgrass beds. One habitat often 
overlooked is high intertidal algal mats: the yellow-green 
alga Vaucheria (Chrysophyta: Xanthophyceae) forms ex- 
tensive mats within the lower marsh, in tidal creeks, and 
on mud flats, downshore from salt marshes. Although 
Vaucheria inhabits and often dominates this habitat in 
many temperate and boreal estuaries in the Northern 
Hemisphere (NIENHUIS & SIMONS, 1971; SIMONS, 1974a, 
b, 1975a, b; JONGE, 1976; POLDERMAN & POLDER- 
MAN-HALL, 1980; GARBARY & FITCH, 1984), basic eco- 
logical information on Vaucheria and its associated inver- 


' Present address: P.O. Box 1995, Newport, Oregon 97365, 
USA. 


tebrate fauna is meager (but see HARTOG & SWENNEN, 
1952; HartToc, 1959). 

The alga is the primary, or even sole, food of three 
species of ascoglossan (= sacoglossan) opisthobranchs. In 
temperate and boreal estuaries throughout the Northern 
Hemisphere, Alderia modesta (Loven, 1844) associates with 
Vaucheria mats (HARTOG, 1959; BLEAKNEY & BAILEY, 
1967; THOMPSON, 1976; BLEAKNEY & MEYER, 1979; MIL- 
LEN, 1980; ROGINSKAJA, 1984; BLEAKNEY, 1988). In the 
N.E. Atlantic Ocean, White Sea, and Barents Sea, the 
ascoglossan Limapontia depressa Alder & Hancock, 1862, 
coexists with A. modesta (THOMPSON, 1976; ROGINSKAJA, 
1984). Finally, Elysta chlorotica Gould, 1870, is an estu- 
arine species endemic to the N.W. Atlantic that associates 
with Vaucheria and the filamentous green alga Cladophora 
(BAILEY & BLEAKNEY, 1967; CLARK, 1975; BLEAKNEY & 
MEYER, 1979; BROMLEY & BLEAKNEY, 1979; GRAVES et 
al., 1979). 

Although the ascoglossans have been examined in many 


Page 304 


Arcata & Humboldt Bays 
Eel River Slough 


Figure 1 


Location of N.E. Pacific estuaries surveyed in this study (solid 
arrows) and several previous studies (hollow arrows; HAND, 1955; 
HAND & STEINBERG, 1955; STEINBERG, 1963). Latitudes and 
longitudes are indicated. 


areas of their geographic ranges, information on Alderia 
modesta in the N.E. Pacific is limited (HAND, 1955; HAND 
& STEINBERG, 1955; STEINBERG, 1963; MILLEN, 1980; 
‘TROWBRIDGE, 1993). The species occurs from Vancouver 
Island, British Columbia (MILLEN, 1980) to Elkhorn 
Slough, California (STEINBERG, 1963). Within this re- 
gional range, A. modesta is reportedly common in at least 
three localities (hollow arrows, Figure 1): Bay Farm Is- 
lands in San Francisco Bay and Elkhorn Slough, Califor- 
nia, and San Juan Island in Puget Sound, Washington 
(HAND, 1955; HAND & STEINBERG, 1955; STEINBERG, 
1963). Yet, quantitative density estimates are lacking, and 
the ascoglossan is not included in most other opisthobranch 
surveys that encompass northern California or Oregon 
shores. Therefore, this study addresses whether A. modesta 
is widely distributed and abundant in N.E. Pacific estu- 
aries. 


NATURAL HISTORY 


Alderia modesta has planktotrophic larvae and _ benthic 
adults. Larvae settle, metamorphose, and recruit to the 
algal hosts during spring, summer, and fall in Atlantic 


The Veliger, Vol. 36, No. 4 


localities (HARTOG, 1959; VADER, 1981), and large adults 
overwinter in marsh ponds (BLEAKNEY & BaILEy, 1967; 
BLEAKNEY & MEYER, 1979; BROMLEY & BLEAKNEY, 1979). 
The ascoglossan grows to sexual maturity about 10 days 
after metamorphosis (SEELEMANN, 1967). Maximum slug 
size ranges from 5 to 16 mm, depending on locality (ENGEL 
et al., 1940; HARTOG, 1959; BLEAKNEY & BAILEY, 1967). 
In the N.E. Pacific, the reported maximum size of A. 
modesta ranges from 6 to 8 mm (HAND & STEINBERG, 
1955; BLEAKNEY, 1988; ‘TROWBRIDGE, 1993). The species 
apparently manifests no endemism or local morpholog- 
ical variation despite its wide geographic distribution 
(BLEAKNEY, 1988). 

Although HartToc (1959) noted that Alderia modesta 
associated with some, but not all, estuarine species of 
Vaucheria, little is known about specific algal-host asso- 
ciations. At least four species of Vaucheria occur in the 
N.E. Pacific (GARBARY & FITCH, 1984; SCAGEL et al., 
1986): V. intermedia and V. thureti are summer to fall 
species whereas V. litorea and V. longicaulis are fall to 
spring species (CONOVER, 1958; NIENHUIS & SIMONS, 1971; 
Simons, 1975a; POLDERMAN & POLDERMAN-HALL, 1980). 
Because the coenocytic algal filaments interweave (JONGE, 
1976), species identification is difficult. Thus, in this study, 
I did not identify the species composing the Vaucheria mats 
examined. 


METHODS anp MATERIALS 
Local Patterns 


Because the alga Vaucheria and ascoglossan Alderia mo- 
desta are not widely recognized as common estuarine spe- 
cies in the N.E. Pacific and because the herbivore occurs 
almost exclusively on or around Vaucheria mats, I collected 
information on the distribution of the alga in Yaquina and 
Coos bays on the central coast of Oregon, USA (Figure 
1). During the summers of 1990 and 1991, I walked the 
shoreline for several hundred meters at every access point 
on the bays, searching for the alga. 

I selected two well-developed regions of algal mats in 
Yaquina Bay for monitoring of Alderia modesta. At each 
of the two sites, I marked 50-m transects directly down- 
shore from the salt marsh. From May 1990 to January 
1992, I surveyed these regions at periodic intervals. During 
each survey, I examined 10 to 52 randomly selected 0.25- 
m? quadrats along each transect line. I counted the number 
of epifaunal A. modesta within each quadrat. Because the 
density of epifaunal ascoglossans declined with increased 
exposure time, I started counting immediately upon aerial 
exposure on ebbing tides. To determine whether A. modesta 
was the major invertebrate associated with the algal mats, 
I also quantified all other taxa encountered in the quadrats. 
Furthermore, in November 1990, I measured the percent 
cover of the Vaucheria beds, width of beds downshore from 
the salt marsh, and height of beds above the adjacent mud 
flat. 


C. D. Trowbridge, 1993 


Regional Patterns 


To evaluate whether the algal-ascoglossan patterns ob- 
served in Oregon were typical of other estuaries in the 
N.E. Pacific, I surveyed Arcata and Humboldt bays and 
Eel River Slough in Humboldt County, California (Figure 
1) in May 1992. Furthermore, I visited Bodega Bay in 
Sonoma County and Tomales and Drakes bays in Marin 
County, California (Figure 1) in July 1990 and May 1992. 
I looked for Vaucheria and Alderia modesta at most of the 
public access points around each bay (based on CALIFORNIA 
COASTAL COMMISSION, 1991). 

In areas that I found the alga, I quantified ascoglossan 
density in 8 to 15 haphazardly selected quadrats (each 625 
cm?) of the lushest, greenest sections of the algal mat, where 
ascoglossans were typically abundant. These values pro- 
vided estimates of peak ascoglossan densities. Next, I 
stretched a 15-m transect line along the Vaucheria zone 
and examined 10 to 15 randomly selected 0.25-m? quadrats 
along each transect. I counted the ascoglossans in each 
quadrat and calculated mean population densities. To fa- 
cilitate comparisons of values from different studies using 
a variety of quadrat sizes (1 dm’ to 1 m’), I present all 
densities of Alderia modesta as numbers per square meter. 
In May 1992, I also measured the maximum size of A. 
modesta at each site to determine the extent to which as- 
coglossan size varied regionally. 

Between-site variation in ascoglossan populations may 
be due to differences in predator assemblages: shorebirds 
appeared to consume Alderia modesta in Norway (VADER, 
1981), and estuarine fishes and shore crabs readily con- 
sumed the ascoglossan in Oregon (Trowbridge, unpub- 
lished data). Therefore, in July 1990 and May 1992, I 
noted the presence or absence of shorebirds and shore crabs 
at each census location. 


RESULTS 


Local Patterns 


Algal distribution: In Yaquina Bay, the alga Vaucheria 
occurred in two areas. On the south shore (Figure 2), the 
alga covered 70-80% of the area along two transects (SE 
and SW) directly below the salt marsh and formed exten- 
sive mats about 150 cm broad and 1.5 to 3 cm tall (above 
the mud flat). On the north shore (N), the Vaucheria bed 
covered only about 10% of the substrate sampled and was 
relatively narrow (about 20 cm) and thin (<1 cm) (Figure 
2). The alga formed discrete “patch islands” below the 
marsh. 

In Coos Bay (Figure 3), the alga was extremely sparse 
(1) near the mouth of the bay where the beaches were 
muddy sand and (2) in many of the sloughs that had pebbly 
to rocky substrate. Much of Coos Bay was highly chan- 
nelized due to logging: the alga occurred only in trace 
amounts within the marsh in these areas. Vaucheria was 
not common where low marsh vegetation (e.g., the pick- 
leweed Salicornia virginica) was missing. 


Page 305 


Vaucheria Beds 


100 


% Cover 
Width (cm) 


50 


. 
a 


Zz 
wn 
res 
nv 
= 


Yaquina Bay, Oregon 
Figure 2 


Description of the Vaucheria beds in Yaquina Bay, Oregon. Data 
were collected in November 1990. Error bars denote +1 SE. 
Values above each bar indicate the number of replicate 0.25-m? 
quadrats examined. 


In South Slough of Coos Bay (Figure 3), however, 
Vaucheria formed extremely thick, lush mats during the 
summer. At the mouth of the slough, the alga formed mats 
fringing the marshes and “patch islands.” The latter were 


Pacific 
Ocean 


.PA? 
BAIR, 
CA 


Alderia modesta > 
none >> 

yarns 

SK ee * 


South Slough 
Figure 3 


Distribution of Alderia modesta in Coos Bay, Oregon, during the 
summer of 1991. Solid arrows denote areas with A. modesta; 
hollow arrows denote areas without the ascoglossan. The star 
denotes the site with peak ascoglossan density (about 5000/m? 
in September 1991). 


Page 306 


800 


700 


600 \ Yaquina Bay 
Oregon 


500 


400 


300 


200 


Alderia Density (#/m’) 


100 
21 25 10 52 


oN PanHerdatI}n097 


Sampling Date 


0 
pass poo7QuiQy 


Figure 4 


Temporal abundance pattern of Alderia modesta on the south side 
of Yaquina Bay (Idaho Point Road), Oregon. Error bars denote 
+ 1 SE. Values above each circle indicate the number of replicate 
0.25-m* quadrats examined. 


stable structures, 15 to 30 m in length, that persisted 
throughout the year. Although the alga was extremely 
sparse on the extensive mud flat flanking the main channel 
of the slough, Vaucheria dominated the substrate directly 
downshore of the marsh vegetation in many of the side 
tributaries. These regions historically had been diked pas- 
tures but subsequently reverted to salt-marsh and mud- 
flat communities. This historical change is typical of many 
estuaries in Oregon and northern California. 


Ascoglossan abundance: Alderia modesta occurred on most 
of the well-developed Vaucheria mats in Yaquina Bay and 
South Slough of Coos Bay. Mean ascoglossan density ranged 
from tens to hundreds per square meter of algal mat. Peak 
densities in individual quadrats were 2152/m? in Novem- 
ber 1990 in Yaquina Bay and about 5000/m/? in September 
1991 in the upper reaches of South Slough (star symbol 
in Figure 3). 

Alderia modesta was present during the entire year (Fig- 
ure 4) except following an abnormally cold storm in De- 
cember 1990 when the temperature dropped below freez- 
ing for a week, and extensive mortalities of intertidal 
invertebrates occurred. In February and March 1991, A. 
modesta populations in Yaquina Bay had not yet recovered: 
no ascoglossans were observed despite extensive searching. 
In South Slough of Coos Bay, however, low densities of 
A. modesta were found on Vaucheria in gaps within the 
marsh vegetation. For example, based on 19 quadrats ex- 
amined (each 625 cm’), mean ascoglossan density was 290/ 
m’ (SD = 368). No ascoglossans were found on exposed 
Vaucheria mats below the South Slough marsh. 

During the following winter, freezing weather did not 


The Veliger, Vol. 36, No. 4 


occur, and Alderia modesta persisted, although the species’ 
distribution was extremely patchy. For example, in Jan- 
uary 1992, few ascoglossans persisted on the Vaucheria bed 
below the marsh on the south side of Yaquina Bay (Figure 
4) although adults did occur in gaps in the marsh vege- 
tation. On the north side of the bay (with a southern 
exposure), however, the algal mats were extremely lush, 
and ascoglossans were abundant: >800/m? based on 10 
haphazardly selected 0.25-m* quadrats. Thus, the seasonal 
persistence of A. modesta in Oregon was associated with 
local variation in microhabitats. 


Invertebrate assemblage: Alderia modesta numerically 
dominated the invertebrate assemblage associated with 
Vaucheria mats. Based on nine pooled censuses from May 
1990 to January 1992 in Yaquina Bay, the ascoglossan 
composed 99% of the epifaunal community (n = 5708 
invertebrates). Insects, particularly larval and adult chi- 
ronomids, were often present on Vaucheria mats, though 
in extremely low densities. 


Regional Patterns 


Distribution: In May 1992, I found little Vaucheria and 
no Alderia modesta at access points of Arcata Bay or the 
nearby Eel River Slough. Both drainage basins were pri- 
marily high-energy environments with marsh banks se- 
verely undercut by erosion. The South Jetty region of 
Humboldt Bay, however, was a low-energy environment 
with trace amounts of Vaucheria and some A. modesta in 
the muddy sand region. The south bay area within the 
US. Fish & Wildlife refuge appeared, from a distance, to 
be ideal for the alga and ascoglossan—a muddy, low- 
energy environment with well-developed marsh vegetation. 
The area, unfortunately, could not be feasibly sampled due 
to limited safe access. Most of the areas visited in Sonoma 
and Marin counties, however, had well-developed Vauche- 
ria mats. 


Abundance: When I haphazardly selected lush portions 
of the algal mats, the density of Alderia modesta (Figure 
5) was moderately high at two sites in California: >100/ 
m’ at Bodega Marine Laboratory Research Reserve in 
Bodega Bay and at Inverness in Tomales Bay. These values 
represent peak abundances calculated from small spatial 
scales (625-cm* quadrats). When I counted ascoglossans 
in randomly selected quadrats (each 0.25 m?), mean A. 
modesta densities ranged from 2 to 20 slugs per square 
meter (Figure 5). Therefore, even though small patches 
of Vaucheria in California had moderate densities of A. 
modesta, randomly determined densities were quite low: 
about 1 to 2 orders of magnitude lower than in Oregon. 


Ascoglossan size: The maximum length of Alderia modesta 
varied little among sites in California and other areas in 
the N.E. Pacific (Table 1). Peak ascoglossan size was 9 
mm in May 1992 at Doran Beach in Bodega Bay, Cali- 
fornia. Although size-frequency data were not collected 
for A. modesta in California, few small individuals were 


C. D. Trowbridge, 1993 


observed. Qualitatively, average ascoglossan size was greater 
in California than in Oregon. 


Potential predators: Small, migrating shorebirds (e.g., 
plovers, sanderlings) were common at many sites in Cal- 
ifornia in July 1990 and May 1992 but generally not 
observed in Oregon estuaries (Table 2). Furthermore, the 
density of shore crabs, particularly the mud-flat crab 
Hemigrapsus oregonensis, was much higher in California 
than in Oregon. I found up to 10 crabs in every quadrat 
surveyed in California and no crabs in quadrats in Oregon. 


DISCUSSION 
Distribution and Abundance 


Local patterns: Alderia modesta was patchily distributed 
on a local scale. Part of this variation was associated with 
the relative abundance of places for the ascoglossans to 
hide during emergence. HARTOG (1959) noted that slug 
densities were low when the Vaucheria bed was closed (2.e., 
tightly interwoven algal filaments) because of the difficulty 
for slugs to burrow and hide. Most A. modesta occurred 
along the margins of cover, around the open spaces in 
vegetation, and in shrinking rents in the substrate during 
emergence (HaARTOG, 1959; C. D. Trowbridge, personal 
observations). Furthermore, I observed that the ascoglos- 
sans hid in surface depressions of the Vaucheria mats, 
invertebrate burrows (crabs, clams, polychaetes), and in 
holes produced by feeding shorebirds. It is not known 
whether Vaucheria mats differing in surface texture rep- 
resent different algal species or a single species under dif- 
ferent environmental conditions. 

Predation by shorebirds and crabs presumably contrib- 


Page 307 


1000 


Haphazard 


Random Z 


100 


10 


Alderia Density (#/m’) 


Figure 5 


Density of Alderia modesta in haphazardly placed and randomly 
selected quadrats. Bodega Marine Laboratory Research Reserve 
and Doran Beach are in Bodega Bay; Inverness is in Tomales 
Bay; Drakes and Limantour esteros are in Drakes Bay, Cali- 
fornia. The symbol “nd” denotes no data collected. Error bars 
denote +1 SE. Values above each bar indicate the number of 
replicate quadrats examined. 


uted to the patchy distribution of ascoglossans. VADER 
(1981) reported that Little Stints (Calidris minuta) regu- 
larly occupied the Vaucheria zone in Norway, and he ob- 
served that the birds consumed Alderia modesta and/or 
their egg capsules. Furthermore, Trowbridge (unpub- 


Table 1 


Maximum reported length of Alderia modesta in the N.E. Pacific. Sample sizes (7) denote number of ascoglossans examined. 
The symbol “na” indicates that sample size was not provided by authors. 


Body length (mm) 


Locations Maximum 


British Columbia 
Bamfield Marine Station 6 


Washington 
Friday Harbor Labs 7 


Oregon 
Yaquina Bay 6 
California 
Doran Beach 
Bodega Marine Lab Reserve 
Inverness 
Drakes Estero 


Limantour Estero 
Elkhorn Slough 


Cow FUN SO 


n References 

12 BLEAKNEY, 1988* 

10 BLEAKNEY, 1988* 
148 ‘TROWBRIDGE, 1993 

27 this studyt 
184 this studyf 
171 this studyt 

18 this studyt 

4 this studyt 
na HAND & STEINBERG, 1955 


* Data not collected for specific purpose of determining maximum length of local population. 


+ Data collected during the May 1992 survey. 


Page 308 


Table 2 


Visual assessment of the abundance of shorebirds and mud- 
flat crabs (Hemigrapsus oregonensis) on Vaucheria in sev- 
eral N.E. Pacific estuaries. Data for Oregon sites were 
based on several months of observations whereas data for 
California sites were based on two surveys (July 1990 and 


May 1992). 
Locations Shorebirds Mud-flat crabs 

Yaquina Bay, Oregon 

Bay Road absent absent* 

Idaho Point Road absent absent* 
Coos Bay, Oregon 

Main Brancht absent absent 

Charleston Bridge absent absent* 

South Slought absent absent 
Bodega Bay, California 

Doran Beach abundant abundant 

Research Reserve abundant abundant 
Tomales Bay, California 

Walker Creek absent absent 

Alan Sieroty Beach absent abundant 

Millerton Point absent abundant 

Inverness abundant abundant 
Drakes Bay, California 

Drakes Estero absent abundant 

Limantour Estero absent very abun- 

dant 


* Low densities of crab burrows observed at site but not in 
quadrats. 
+ Many locations pooled (see Figure 3). 


lished data) found that predators (probably fishes and crabs 
but not birds) significantly reduced populations of A. mo- 
desta in Yaquina Bay, Oregon. Yet, although predation 
may reduce ascoglossan densities, the burrowing behavior 
and small size of A. modesta presumably would offer some 
protection from predators: total exclusion of ascoglossans 
seems unlikely. 

Another potentially important source of variability in 
slug density was the recruitment rate of larval ascoglossans. 
Information on patterns of water circulation and larval 
transport within N.E. Pacific estuaries is limited. Water 
masses containing larvae may not penetrate all the trib- 
utaries of the estuaries (e.g., Walker Creek near the mouth 
of Tomales Bay), thus explaining the absence of Alderia 
modesta. Alternatively, abiotic factors such as salinity fluc- 
tuations may exclude ascoglossans from some locations. 
ENGEL et al. (1940) reported that A. modesta can survive 
at salinities from about 2 to =37%o though the effects of 
low salinity on ascoglossan growth and fecundity are not 
known. 


Regional patterns: Alderia modesta was often abundant, 
ranging from tens to thousands of animals per square meter 
throughout its geographic range. For example, HARTOG 
(1959) reported 20 to 56 individuals per square meter in 


The Veliger, Vol. 36, No. 4 


10000 
= 8000 
SS 
= 
> 6000 Oregon 
a oO 
A 4000 
“2 Oregon / ® Netherlands 
a 2000 


Germany 
0 AB California 
30 40 50 60 #70 + 80 


Latitude (° N) 
Figure 6 


Relationship between peak ascoglossan density and latitude. Data 
are from this study (Oregon, California) and previous studies 
(HaRTOG, 1959; SEELEMANN, 1967; VADER, 1981). 


the Netherlands with a peak density of 3100/m?. SEELE- 
MANN (1967) observed 1400/m? on the German Baltic 
coast. VADER (1981) reported that densities of 500 to 1500 
ascoglossans/m? were typical of most sites in Norway; at 
Klubbukt, however, the mean density was 4820/m? with 
a peak value of 9000/m?. Density values for Oregon and 
California were, therefore, comparable to values from N.E. 
Atlantic localities. 

CLarRK & DE FREESE (1987) reported an increase in 
multispecies ascoglossan density from low to high latitudes. 
A similar pattern was seen for a single species (Alderia 
modesta, Figure 6). The correlation was highly significant 
(r = 0.825, P = 0.012, n = 8 sites) even though the data 
were from different locations, years, and seasons as well 
as based on different sample and quadrat sizes. At least 
three factors may account for the latitudinal trends in 
population density: (1) decrease in predation intensity, (2) 
increase in algal productivity (CLARK & DE FREESE, 1987), 
or (3) increase in larval recruitment with increased lati- 
tude. This study provides some evidence supporting (1), 
but predation was not the sole factor. Although Vaucheria 
beds were generally lusher in Oregon than California, 
algal productivity probably did not constrain ascoglossan 
populations in California for two reasons. First, the alga 
was not a limiting resource for the ascoglossans. Second, 
maximum body length did not differ much for populations 
throughout the N.E. Pacific (Table 1). The paucity of 
juvenile ascoglossans in California and abundance of small 
individuals in Oregon (TROWBRIDGE, 1993) support the 
recruitment hypothesis (3). The relative importance of 
predation intensity, algal quality (as food and substratum), 
and larval recruitment need to be further elucidated for 
us to understand regional differences in ascoglossan pop- 
ulations. 


C. D. Trowbridge, 1993 


Ecological Effects 


As the numerically dominant invertebrate associated with 
Vaucheria mats, Alderia modesta has two ecological roles 
within the estuarine food web: (1) as a stenophagous con- 
sumer and major herbivore of the algal mats and (2) as 
prey for estuarine predators. Ascoglossan herbivory may 
be important to algal hosts under conditions of high feeding 
rates and/or high population densities (CLARK, 1975; 
TROWBRIDGE, 1992). Information on feeding rates of 
A. modesta are meager. EVANS (1953) commented on the 
rapid feeding rate of the ascoglossan: 10 Vaucheria fila- 
ments per minute. This value, however, is difficult to eval- 
uate because filament size was not given. Because herbiv- 
ory may be important to algal hosts when ascoglossan 
density is high, ascoglossan herbivory in Oregon estuaries 
may contribute to the periodic fragmentation of Vaucheria 
mats. 

High densities of Alderia modesta in Oregon estuaries 
suggest that ascoglossans may represent an important food 
source to estuarine fishes, crabs, and perhaps birds. Al- 
though predators rapidly reduced densities of A. modesta 
in August 1990 in Yaquina Bay (Trowbridge, unpublished 
data), feeding preferences of predators may change onto- 
genetically or seasonally. For example, small (<10 cm) 
staghorn sculpins (Leptocottus armatus) voraciously con- 
sumed A. modesta whereas larger conspecific fish (> 15 cm) 
ignored the small opisthobranchs (Trowbridge, unpub- 
lished data). Thus, the ascoglossan may be either (1) an 
important food base within high intertidal, estuarine hab- 
itats or (2) a minor prey base sampled by a diverse array 
of inexperienced juvenile predators. In summary, the eco- 
logical role of A. modesta merits further attention, partic- 


ularly at high latitudes where ascoglossan densities are 
high. 


ACKNOWLEDGMENTS 


Access to the estuarine reserves was kindly granted by S. 
Rumrill (South Slough National Estuarine Research Re- 
serve), Peter Conners (Bodega Marine Laboratory Re- 
search Reserve), and K. Forester (U.S. Fish & Wildlife 
Service, Humboldt Bay National Wildlife Refuge). I thank 
K. Forester and T. Gosliner for suggesting potential sam- 
pling locations and H. Ross, C. B. Trowbridge, and P. 
Schreter for field assistance. K. Clark and an anonymous 
reviewer made constructive comments on an earlier draft 
of this manuscript. The writing of this manuscript was 
supported by the Leigh Marine Laboratory, University of 
Auckland and a National Science Foundation grant (INT- 
88888850OR0) to the author. 


LITERATURE CITED 


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BLEAKNEY, J. S. 1988. The radula and penial style of Alderia 
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BLEAKNEY, J. S. & K. B. MEYER. 1979. Observations on salt- 
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CxiarK, K. B. & D. DE FREESE. 1987. Population ecology of 
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Conover, J.T. 1958. Seasonal growth of benthic marine plants 
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ENGEL, H., S. J. GEERTS & C. O. VAN REGTEREN ALTENA. 
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Evans, T. J. 1953. The alimentary and vascular systems of 
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GarBaRY, D. J. & R. S. FitcH. 1984. Some brackish species 
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130. 

GRAVES, D. A., M. A. GIBSON, & J. S. BLEAKNEY. 1979.. The 
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HAaAnp, C. 1955. Alderia modesta in Washington. The Nautilus 
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HAND, C. & J. STEINBERG. 1955. On the occurrence of the 
nudibranch Alderia modesta (Lovén, 1844) on the central 
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HartToc, C. DEN. 1959. Distribution and ecology of the slugs 
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HarToc, C. DEN & C. SWENNEN. 1952. On the occurrence of 
Alderia modesta (Lovén) and Limapontia depressa A. & H. 
on the salt marshes of the Dutch Wadden Sea. Beaufortia 
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JonceE, V.N.pDE. 1976. Algal vegetations on salt-marshes along 
the western Dutch Wadden Sea. Netherlands Journal of Sea 
Research 10:262-283. 

MILLEN, S. V. 1980. Range extensions, new distribution sites, 
and notes on the biology of sacoglossan opisthobranchs (Mol- 
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of Zoology 58:1207-1209. 

NIENHUIS, P. H. & J. SIMONS. 1971. Vaucheria species and 
some other algae on a Dutch salt marsh, with ecological 
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POLDERMAN, P. J. G. & R. A. POLDERMAN-HALL. 1980. Algal 


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RocinskaJA, I. S. 1984. The species composition and pecu- 
liarities of the ecology of the Sacoglossa in the Barents Sea 
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SCAGEL, R. F., D. J. GARBARY, L. GOLDEN & M. W. HAWKES. 
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cological Contribution 1, University of British Columbia: 
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SEELEMANN, U. 1967. Rearing experiments on the amphibian 
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Simons, J. 1974a. Vaucheria birostris n. sp. and some further 
remarks on the genus Vaucheria in the Netherlands. Acta 
botanica neerlandica 23:399-413. 

SIMONS, J. 1974b. Vaucheria compacta: a euryhaline estuarine 
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SIMONS, J. 1975b. Vaucheria species from estuarine areas in 
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83:207-220. 

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The Veliger 36(4):311-316 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


The Influence of Olfactory and ‘Tactile 


Stimuli on the Feeding Behavior of 
Melibe leonina (Gould, 1852) 
(Opisthobranchia: Dendronotacea) 


by 


WINSOR H. WATSON IIT! 


AND 


CHARLES M. CHESTER 


Zoology Department, Coastal Marine Laboratory, Center for Marine Biology, 
University of New Hampshire, Durham, New Hampshire 03824, USA 


Abstract. 


The nudibranch Melibe leonina feeds using the rhythmic movements of its large oral hood 


to capture small crustaceans that are present in the water column. The frequency of these feeding 
movements, or hood closures, is proportional to the concentration of available prey. The purpose of this 
study was to determine what qualities of prey cause the rate of these feeding movements to change. 
Animals were observed during exposure to the following treatments: (1) filtered seawater; (2) Artemia- 
conditioned seawater (smell); (3) small particles in seawater; (4) particles soaked in Artemia-conditioned 
seawater; (5) frozen Artemia and; (6) live Artemia. Both conditioned water and particles caused appetitive 
behavior (orientation of the oral hood) and a significant increase in the frequency of hood closures. ‘This 
increase in rate had a rapid onset and was maintained throughout the duration of the 20-min test period. 
The major difference between the effects of the two stimuli was that smell alone led to incomplete 
feeding cycles while particle treatments yielded normal feeding behavior. When applied together these 
stimuli produced a larger response than either one did alone. However, no combination of stimuli was 
as effective as live prey. We conclude that both tactile and chemical cues are sufficient to elicit an increase 
in the feeding movements of Melibe leonina, but some additional stimulus provided by live prey, such 
as vibrations, may play an important role as well. The information provided by these stimuli helps 
initiate appetitive and early aspects of the consummatory phases of feeding, and also influences full 
expression of the rhythmic feeding motor program. 


INTRODUCTION 


In most mollusks, both chemical and tactile stimuli have 
a strong influence on feeding behavior (KOHN, 1983; 
AUDESIRK & AUDESIRK, 1985). The presence of chemo- 
receptors in the oral region of many mollusks has been 
well documented, as has the ability of food extracts to elicit 
both the appetitive and consummatory phases of feeding 


''To whom requests for reprints should be sent at Zoology 
Department, U.N.H., Durham, New Hampshire 03824. 


(KOHN, 1961; CROLL, 1983). Mechanoreceptors, which 
often have centrally located somata, are found both around 
the mouth and in various regions of the esophagus and 
gut, and they appear to be capable of either exciting or 
inhibiting feeding and swallowing behaviors. However, the 
relative influence of each type of stimulus on feeding be- 
havior has only been examined closely in a few species. 
In Aplysia, as in many mollusks, there is a clear appe- 
titive response to the presence of chemical stimuli (PRESTON 
& LEE, 1973; KUPFERMANN, 1974). Animals wave their 
head, and lift the anterior two-thirds of their body off the 


Page 312 


substrate. If head waving does not bring them in contact 
with food, they alternate locomotion and head waving until 
food is localized. Chemical stimuli alone (seaweed extract), 
when applied to the lips, or mouth region, will elicit a 
biting response, while tactile stimuli alone (a glass rod) 
will not (ROSEN et al., 1982). Nevertheless, tactile stimuli 
will enhance the response to chemical input, resulting in 
regular biting. 77ztonia diomedea (Bergh, 1894) also bites 
repeatedly in response to chemical input (sea whip extract), 
and as with Aplysza, tactile stimuli in the mouth or esoph- 
agus modulates this behavior (AUDESIRK & AUDESIRK, 
1979). Some interesting mechanoreceptor cells, which also 
receive excitatory chemical input from the oral veil and 
mouth region, appear to be at least one site where the two 
modalities might undergo peripheral integration (AUDES- 
IRK & AUDESIRK, 1980a, b). 

The dendronotacean opisthobranch Melibe leonina 
(Gould, 1852) is an unusual gastropod lacking jaws, a 
radula, and a well-defined buccal mass (GOSLINER, 1987). 
It feeds by removing small planktonic animals from the 
water column using a specialized oral hood (AGERSBORG, 
1921; Hurst, 1968; AJEskKA & NYBAKKEN, 1976). This 
structure 1s equipped with sensory, muscular, and vascular 
elements that allow for the efficient capture of free-swim- 
ming prey (HursT, 1968). The oral hood surrounds prey 
that are in the water column, closes to force water out 
through the tentacles on the edge of the veil, and then 
contracts further to bring the captured animals into the 
mouth (WATSON & TRIMARCHI, 1992). If sufficient prey 
are available, the behavior is rhythmic, with a frequency 
ranging from 0.5 to 3 cycles/min, depending on the con- 
centration of food in the water (WATSON & TRIMARCHI, 
1992). 

At the present time little is known about the motor 
programs underlying expression of rhythmic feeding in 
Melibe, or the sensory inputs that control and influence 
their expression. The fact that the feeding rhythm is ste- 
reotyped (WATSON & TRIMARCHI, 1992), and occurs with 
a slow rhythm in the absence of prey (AJESKA & NYBAKKEN, 
1976; THOMPSON & CRAMPTON, 1984) suggests that a 
central pattern generator may be involved. Melibe is sen- 
sitive to tactile stimulation (BICKELL & KEMPF, 1983) and 
there is some evidence that the feeding cycles are triggered 
by contact of prey with the oral hood (Hurst, 1968). 
However, no information is available about the possible 
role of chemoreceptors. The hypothesis put forth by 
WATSON & ‘TRIMARCHI (1992) is that the feeding rhythm 
is under the control of a central pattern generator (CPG), 
and both chemical and tactile stimuli modulate this CPG. 
The goal of this study was to determine the relative influ- 
ence of chemical and mechanical stimuli on Melibe feeding 
behavior. 


MATERIALS anpD METHODS 


All animals were collected, using SCUBA, from an eelgrass 
bed located along the border of the San Juan Channel, 
iear an area of Shaw Island called Neck Point. Shaw 


The Veliger, Vol. 36, No. 4 


Island is part of an archipelago of 172 islands in the upper 
Puget Sound, Washington, known collectively as the San 
Juan Islands. Animals were shipped to New Hampshire 
and maintained in recirculating aquaria at 10-15°C, in 
the Zoology Department, U.N.H., Durham, New Hamp- 
shire. Animals were starved at least 7 days prior to testing. 
Feeding experiments were performed in a 15-L aquarium, 
at 12°C. Three to four animals were placed in the aquar- 
ium and allowed to acclimate for 30 min. The feeding 
activity of each animal (number of hood closures/min) was 
monitored for 20 min before and throughout each 20-min 
treatment. In addition, we determined whether each feed- 
ing act was complete, according to the criteria described 
by WATSON & TRIMARCHI (1992). This allowed us to 
calculate the percent of feeding cycles that were prema- 
turely terminated for each treatment. 

Animals were exposed to the following substances: (1) 
filtered seawater (control); (2) water conditioned with Ar- 
temia (smell); (3) small (350 um) Sephadex beads in fil- 
tered seawater (particles); (4) Sephadex beads soaked over- 
night in Artemia-conditioned seawater (smell and particles); 
(5) frozen Artemia; and (6) live Artemia. Stimuli were 
added as concentrated 50-mL aliquots so that when they 
were diluted in the 15-L aquarium, a final concentration 
of 1500 particles, or Artemiza/ L, or the odor equivalent 
to 1500 Artemia/L, was obtained. Although Artemia is not 
a normal component of the diet of Melibe it was used as 
a food source because it provides a well-defined and quan- 
tifiable diet, and our subjects ate them as voraciously as 
natural prey. Several preliminary studies with natural prey 
yielded comparable results. 

Statistical analyses were performed using the program 
SYSTAT (SYSTAT Inc., Evanston, II.). Ten Melibe were 
randomly chosen for each treatment. The effects of each 
treatment on complete and on incomplete feeding cycles 
were analyzed using a one-way analysis of variance (ANO- 
VA) model (SOKAL & ROHLF, 1981). In some cases data 
were In (x + 1) transformed to uncouple the variance from 
the mean and to give a positive value (KREBS, 1989). A 
Student-Newman-Keuls multiple comparison was used to 
detect differences between treatments. To compare the con- 
trol with individual stimuli, ¢-tests were utilized. 

In some experiments animals were sequentially exposed 
to different treatments to more accurately compare the 
relative responsiveness of individuals to different stimuli. 
For example, after 20 min exposure to control conditions, 
animals were subjected to a 20 min period during which 
only particles were present, followed by 20 min exposure 
to smell and particles. These treatments were not inde- 
pendent and were not used for statistical analysis. Rather, 
they provided information about the additive effects of 
stimuli and the time course of their influences. 


RESULTS anp DISCUSSION 


In the absence of any stimuli, in control seawater, Melibe 
maintained a hood closure rate of 0.20 cycles/min (n = 
51, SEM = 0.017). None of the controls for the various 


W. H. Watson III & C. M. Chester, 1993 


treatments was significantly different from each other 
(ANOVA F = 1.854, df: 5, 54 P = 0.122). This allowed 
comparisons between experimental treatments to be made. 
The addition of Artemiza-conditioned water (smell) caused 
a significant, and rapid, increase in rate (¢ = 2.79 df = 18, 
P = 0.0016) (Figures 1, 2, 3). This elevation in rate was 
maintained for approximately 15 min, before beginning 
to decline. All the Melibe tested (n = 10) became more 
active and oriented their oral hood toward the source of 
the stimulus. The majority (70%) of the animals tested 
also began to swim shortly after application of the stimulus. 
However, this swimming activity was transient, lasting 2- 
7 min. 

The addition of a tactile stimulus (Sephadex beads, par- 
ticles) also caused a significant increase in hood closure 
rate (¢ = 3.318, df = 18, P = 0.006) (Figures 1, 2, 3). As 
observed with the olfactory stimulus, animals oriented with 
their oral veil facing the source of the particles, and in 
30% of the cases they swam for periods of time ranging 
from 1 to 9 min. In contrast to their response to the ol- 
factory stimulus, a high hood closure rate was maintained 
throughout the observational period. 

There was no significant difference between the effec- 
tiveness of odor and particles as feeding stimulants, al- 
though the rate obtained in the tactile treatment was slight- 
ly higher (Figures 1, 2). Both treatments resulted in 
increases in hood closure rate that were approximately 
one-third as great as those obtained when live food was 
present (Figure 2). In order to try and mimic the stimuli 
present when real prey is available, we exposed animals 
to smell and particles together, particles soaked in Artemia- 
conditioned water, or frozen Artemia. These treatments did 
elicit greater responses than either stimulus applied alone, 
but there was no significant difference between the soaked 
particle, frozen Artemia, or inert particle treatment (Figure 
2). Moreover, none of these treatments was nearly as ef- 
fective as live prey. Thus, both tactile and chemical cues 
are sufficient to elicit an increase in the rate of feeding 
movements of Melibe leonina, but some additional stimulus 
provided by live prey, such as vibrations, probably plays 
an important role as well. 

In order to determine if olfactory and tactile stimuli had 
additive influences on feeding movements we examined the 
effects of adding them sequentially. Both treatments, by 
themselves, resulted in a rapid increase in hood closure 
rate (Figure 3). However, the addition of a second, dif- 
ferent stimulus, 20 min after the initial stimulus, did not 
result in any further increase in the hood closure rate of 
the animals tested. In contrast, addition of live prey to the 
observation chamber, produced a significant increase in 
rate. The findings of this experiment reinforce the hy- 
pothesis that live prey provide an additional feeding stim- 
ulus which excites Melibe feeding activity more than any 
combination of smell or inert particles. 

WATSON & TRIMARCHI (1992) proposed that the feed- 
ing motor program of Melibe consists of a central pattern 
generator which is modulated and regulated throughout 
the feeding cycle by sensory input. They noted that animals 


Page 313 


1.5 
1.2 
1.0 


0.7 


Hood Closures/Minute 


0.5 ——| 
0.2 Sf — 
0.0 
oe = %o Go © © cs £& © 
i o i _ tS _ i he rs > 
~ ~ (5) ~ *) ~~ N ~ a 
e E£& & BS ey 8O Ff 
on Or. ° a ° & ° 
S) OS Gg OS @& YS 
Ay i" 
+ 
v 
E 
n 
Figure 1 


The influence of olfactory and tactile stimuli on the feeding 
frequency of Melibe. Five separate experiments are depicted in 
this figure, each with separate controls. In the first experiment 
animals were exposed to Artemia-conditioned water (smell), in 
the second Sephadex beads (particles), the third particles soaked 
in Artemia-conditioned water, the fourth frozen Artemia, and in 
the final experiment animals were exposed to live Artemza. In all 
cases we observed a significant increase in their rate of hood 
closures following the addition of one of the stimulants. Bars 
represent standard error of measurement. 


often prematurely terminate feeding cycles if food is not 
present. We also observed this phenomenon in our exper- 
iments. When animals were stimulated to feed with an 
olfactory stimulus they increased their hood closure rate, 
but they rarely completed a feeding cycle; more than 70% 
of the feeding cycles they initiated ended before reaching 
the final consumption phase (Figure 4). This proportion 
of incomplete episodes was comparable to that observed in 
controls; however, the feeding movements of control ani- 
mals are much less frequent and regular. In contrast, all 
the treatments that provided something to consume, wheth- 
er inert or otherwise, resulted in a high proportion of 
complete feeding cycles, and consumption of the objects. 
As in our other experiments, live prey were the most ef- 
fective stimuli. Therefore, it appears as if the type of stimuli 
present influence both the rate of food capture and the 
sequential expression of movements associated with food 
acquisition and consumption. 

Adult Melibe are normally found in eelgrass beds or 
kelp forests, where they feed on epifaunal crustaceans, or 
planktonic crustaceans such as copepods and nauplii. Like 
most gastropods their vision is limited and therefore they 
must rely heavily on olfaction and mechanoreception to 
locate food and discriminate appropriate prey from other 
objects. Our laboratory studies indicate that Melzbe is sim- 


Page 314 


1.2 
1.0 
0.8 
0.6 


0.4 


(In(x+1l)episodes/minute) 


Rate of Hood Closure 


0.2 


The Veliger, Vol. 36, No. 4 


0.0 = es a “A i—| eo 
[—) — eo © eo > 
fe o _ ray N te 
- eo 
= =| om oat ) — 

~ he 

° Kd) = be 
om 

=) = O] 

a a. 

+ 

o 

E 

an 

Figure 2 


The relative potency of various feeding stimulants. Overall, the treatments were significantly different from each 
other (ANOVA F = 44.133, df: 5, 54, P > 0.0001). Horizontal lines indicate treatments that are not statistically 
significant from each other, using the Student-Newman-Keul’s multiple comparison test. Both olfactory and tactile 
stimuli enhance feeding frequency to a limited extent, but neither stimulus alone, or when combined with each 
other (smell and particles, frozen Artemia), are as effective as live animals. The data were transformed using the 
natural log of (x + 1). Bars represent standard error of measurement. 


ilar to other gastropods in their use of chemoreceptors to 
initiate appetitive aspects of feeding such as changes in 
locomotion and orientation toward the source of food 
(KUPFERMANN, 1974; CROLL, 1983; AUDESIRK & AUDES- 
IRK, 1985; TEYKE ef al., 1992). It has been suggested that 
chemical stimuli serve primarily to evoke a food-induced 
state of arousal in Aplysia (KUPFERMANN et al., 1991), and 
it may serve a similar role in Melibe as well. Chemical 
stimuli cause Melibe to change their rate of locomotion, 
orient toward the source of the stimuli, and increase their 
rate of feeding movements. However, it appears as if they 
are merely sampling the water, not feeding, because they 
do not carry out complete feeding cycles. This increase in 
the frequency of hood movements may also serve to enhance 
the ability of putative chemoreceptors on the oral veil to 
detect prey; comparable to antennule flicking in many 
crustaceans. Then, once preylike objects make contact with 
the oral hood, they are captured and brought in contact 
with the mouth, and normal feeding behavior is initiated. 

Most opisthobranchs are well endowed with chemo- and 
mechanoreceptors (CROLL, 1983) and it has been postu- 
lated that these two groups of receptors converge on neu- 
rons which regulate different aspects of feeding (ROSEN et 
al., 1982). Evidence from Tvitonia also indicates that some 
mechanoreceptors receive direct input from chemorecep- 


tors which modulates their responsiveness (AUDESIRK & 
AUDESIRK, 1980a), as well as input from some aspect of 
the swim circuit (AUDESIRK & AUDESIRK, 1980b). Thus 
a certain amount of integration and discrimination appears 
to take place very early in the circuit which links sensory 
input to the feeding circuit, and as a result the presence 
of certain odors can have an important impact on the 
responsiveness of the animal to tactile stimulation. This 
appears to be the case in Aplysia (ROSEN et al., 1982) and 
certain other gastropods, where the biting response to me- 
chanical stimuli is limited unless a chemical cue is also 
present. In some cnidarians chemical cues actually alter 
the tuning properties of mechanoreceptors involved with 
prey capture. WATSON & HESSINGER (1989) found that 
the receptors controlling the discharge of sea anemone 
nematocysts are activated by 30-75 Hz vibrations and the 
chemical cues associated with prey modulate these recep- 
tors so they shift their sensitivity to a range of 5-40 Hz, 
which precisely matches the swimming movements of their 
prey (they also used Artemia in their study). In our ex- 
periments it was clear that live Artemia stimulated feeding 
much more effectively than any combination of odor and 
touch. We are presently searching for receptors in Melibe 
that are most sensitive to the vibrations produced by swim- 
ming prey. The possibility that these receptors are also 


W. H. Watson III & C. M. Chester, 1993 


A us Smell Particles Food 


Hood Closures/Minute 


0 10 20 30 40 50 60 70 80 
Time Interval (Minutes) 


B Particles Smell Food 
1.2 | | I 


Hood Closures/Minute 


0 10 20 30 40 50 60 70 80 
Time Interval (Minutes) 


Figure 3 


The response of Melibe to sequential addition of olfactory and 
tactile stimulants. A. After 20 min in filtered seawater, condi- 
tioned water (smell) was added to the observation tank, resulting 
in a rapid increase in feeding frequency, which was maintained 
for 20 min. Addition of particles did not cause any further increase 
in feeding rate during the next 20 min. However, live prey (food) 
had a much greater effect on feeding than the combination of 
particles and food odor. B. This experiment was similar to the 
one described in A, except particles were added first, followed 
by smell, and then live prey (food). As in A, addition of a second 
feeding stimulant did not cause any additional increase in feeding 
rate, while live prey did. Bars represent standard error of mea- 
surement. 


modulated by the odor of prey, or the behavioral state of 
the animals, is also a subject worthy of further investi- 
gation. 

The stereotyped, rhythmic movements involved in Me- 
lube feeding behavior have characteristics typical of fixed 
action patterns that are under the control of a central 
pattern generator or motor program (AJESKA & NYBAKKEN, 
1976; WATSON & TRIMARCHI, 1992). This motor program 
is expressed at a very low frequency (0.2 cycles/min) even 
in the absence of prey, and when it senses prey, through 
a combination of the cues discussed in this paper, the 


Page 315 


na 
eve 
a) 
} 
wo 2 
a 
ve 
== 
E oo 
og 
| 
£s 
eo 
4 is 
—_ = eo 
3 = ° rf S > 
—_ —= N — 
= = 2 a4 ° =) 
S ce L L a 
1S) a «6 
Ay -*) 
+ 
ir) 
=| 
n 
Figure 4 


The influence of feeding stimulants on the sequential expression 
of Melibe feeding movements. The typical Melibe feeding cycle 
consists of a series of movements designed to capture prey and 
bring them in close proximity to the mouth for consumption. If 
prey are sparse or absent, animals often terminate a feeding cycle 
before the tilt and squeeze phase of the cycle, which brings food 
to the mouth. This figure shows the proportion of such prema- 
turely terminated feeding cycles during different treatments. It 
is clear that while the odor of prey stimulates feeding activity 
(Figures 1, 2), the type of feeding movements displayed are sel- 
dom complete. In contrast, when any type of particle is present, 
animals usually attempt to engulf the objects they capture, re- 
sulting in complete feeding cycles. 


cycling rate of the motor program increases. In addition, 
the quality and quantity of sensory input appear to influ- 
ence the full expression or completeness of the feeding 
cycle. If only the odor of food is present, animals become 
aroused and sample the water column for food, often ter- 
minating their feeding cycle prior to making the movements 
that normally bring prey in close proximity to the mouth. 
However, if particles are present, or live prey, most feeding 
cycles are complete. We hypothesize that Melibe feeding 
behavior consists of a series of flexible motor programs 
that are centrally programmed, triggered by sensory input, 
and modulated by sensory feedback throughout the feeding 
cycle. This hypothesis is derived, in part, from an emerging 
view of central pattern generators as broader more flexible 
motor pattern networks, which combine elements of tradi- 
tional motor programs with a high level of sensory mod- 
ulation (HARRIS-WARRICK & Johnson, 1989). Our present 
studies are designed to test this hypothesis and examine 
this relatively new view of “stereotyped” behavior. 


ACKNOWLEDGMENTS 


We wish to thank David Duggins for supplying healthy, 
cooperative animals and Suzanne Watson for her contin- 
ued support and constructive suggestions. This study was 
supported by NIH Grant NS29555 to Dr. Winsor H. 


Page 316 


Watson III. It is contribution number 283 of the Center 
for Marine Biology/ Jackson Estuarine Laboratory series. 


LITERATURE CITED 


AGERSBORG, H. P. K. 1921. Contribution to the knowledge of 
the nudibranchiate mollusc, Melibe leonina (Gould). Amer- 
ican Naturalist 55:223-253. 

AJeSsKA, R. A. & J. NYBAKKEN. 1976. Contributions to the 
biology of Melibe leonina (Gould, 1852). The Veliger 19:19- 
26. 

AUDESIRK, T. & G. AUDESIRK. 1979. Oral mechanoreceptors 
in Tritonia diomedea. II. Role in feeding. Journal of Com- 
parative Physiology 130:79-86. 

AUDESIRK, G. & T. AUDESIRK. 1980a. Complex mechanore- 
ceptors in Tritonia diomedea. II. Neuronal correlates of a 
change in behavioral responsiveness. Journal of Comparative 
Physiology 141:111-122. 

AUDESIRK, T. & G. AUDESIRK. 1980b. Complex mechanore- 
ceptors in Tritonia diomedea. I. Responses to mechanical and 
chemical stimuli. Journal of Comparative Physiology 141: 
101-109. 

AUDESIRK, T. & G. AUDESIRK. 1985. Behavior of gastropod 
molluscs. Pp. 2-84. In: A. O. D. Willows (ed.), The Mol- 
lusca, Neurobiology and Behavior, Vol. 8, Part 1. Academic 
Press: New York. 

BICKELL, L. R. & S.C. KEMpr. 1983. Larval and metamorphic 
morphogenesis in the nudibranch Melibe leonina (Mollusca: 
Opisthobranchia). Biological Bulletin 165:119-138. 

CROLL, R. P. 1983. Gastropod chemoreception. Biological Re- 
view 58:293-319. 

GOSLINER, T. M. 1987. Review of the nudibranch genus Melibe 
(Opisthobranchia: Dendronotacea) with descriptions of two 
new species. The Veliger 29:400-414. 

HARRIS-WarRRICK, R. M. & B. R. JOHNSON. 1989. Motor 
pattern networks: flexible foundations for rhythmic pattern 
production. Pp. 51-71. In: T. J. Carew & D. B. Kelley 
(eds.), Perspectives in Neural Systems and Behavior. Alan 
R. Liss, Inc.: New York. 


The Veliger, Vol. 36, No. 4 


Hurst, A. 1968. The feeding mechanism and behaviour of the 
opisthobranch Melibe leonina. Symposium of the Zoological 
Society of London 22:151-166. 

Koun, A. J. 1961. Chemoreception in gastropod molluscs. 
American Zoologist 1:291-308. 

Koun, A. J. 1983. Feeding biology of gastropods. Pp. 2-61. 
In: A. 8. M. Saleuddin & K. M. Wilbur (eds.), The Mol- 
lusca, Physiology, Vol. 5, Part 2. Academic Press: New York. 

Kress, C. J. 1989. Ecological Methodology. Harper and Row: 
New York. 654 pp. 

KUPFERMANN, I. 1974. Dissociation of the appetitive and con- 
summatory phases of feeding in Aplysia: a lesion study. Be- 
havioral Biology 10:89-97. 

KUPFERMANN, I., T. TEYKE, S. C. ROSEN & K. R. WEIss. 1991. 
Studies of behavioral state in Aplysia. Biological Bulletin 
180:262-268. 

PRESTON, R. J. & R.M. LEE. 1973. Feeding behavior in Aplysia 
californica. Role of chemical and tactile stimuli. Journal of 
Comparative and Physiological Psychology 82:368-381. 

Rosen, S. C., K. R. Weiss & I. KUPFERMANN. 1982. Cross- 
modality sensory integration in the control of feeding in 
Aplysia. Behavioral and Neural Biology 35:56-63. 

SOKAL, R. R. & F. J. ROHLF. 1981. Biometry. 2nd ed. W. H. 
Freeman and Company: New York. 859 pp. 

TEYKE, T, K. R. WEIss & I. KUPFERMANN. 1992. Orientation 
of Aplysia californica to distant food sources. Journal of Com- 
parative Physiology A 170:281-289. 

TuHompson, T. E. & D. M. CRAMPTON. 1984. The biology of 
Melibe fimbriata, a conspicuous opisthobranch molluscs of 
the Indian Ocean, which has now invaded the Mediterranean 
Sea. Journal of Molluscan Studies 50:113-121. 

Watson, W. H., III & J. TRIMARcHI. 1992. A quantitative 
description of Melibe feeding behavior and its modification 
by prey density. Marine Behavioral Physiology 19:183-194. 

Watson, G. M. & D. A. HESSINGER. 1989. Cnidocyte mech- 
anoreceptors are tuned to the movements of swimming prey 
by chemoreceptors. Science 243:1589-1591. 


The Veliger 36(4):317-322 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Ecological, Morphological, and Genetic Differences 


Between the Sympatric Bivalves Donax variabilis 
Say, 1822, and Donax parvula Philippi, 1849 


by 


WALTER G. NELSON 


Department of Oceanography, Ocean Engineering and Environmental Science, 
Florida Institute of Technology, Melbourne, Florida 32901, USA 


ERIK BONSDORFF 


Department of Biology and Husé Biological Station, Abo Akademi University, 
20500 Abo, Finland 


AND 


LAURA ADAMKEWICZ 


Department of Biology, George Mason University, Fairfax, Virginia 22030, USA 


Abstract. 


To clarify the status of Donax variabilis Say, 1822, and D. parvula Philippi, 1849, as 


separate species, comparisons of measurements of shell characteristics, spatial distribution patterns, and 
allozyme frequencies were made on sympatric populations from Melbourne Beach, Florida, USA. A 
significant difference in the regression slopes of shell width versus shell height was found, although 
there was overlap in the data for most of the size range of the specimens examined. The angle of the 
dorsal margins of the shell immediately anterior and posterior to the umbo provided a clear separation 
of the species. Marked differences in frequencies of alleles, but no unique alleles, were found for the 
two species. While D. parvula tended to be distributed more subtidally than D. variabilis, this pattern 
varied with season and there was little spatial separation of the species particularly during spring and 
fall. The balance of evidence indicates that D. variabilis and D. parvula are separate, but highly similar 


species. 


INTRODUCTION 


The taxonomy of the species of the genus Donax along the 
Atlantic coast of the United States was revised by MORRISON 
(1971). Within the region from Ocracoke, North Carolina, 
to St. Lucie County, Florida, Morrison recorded two sym- 
patric species, Donax variabilis Say, 1822, and Donax par- 
vula Philippi, 1849. Donax variabilis has a greater range, 
extending from the coast of Virginia to the coast of Mis- 
sissippi. Following the taxonomic divisions of MORRISON 
(1971), a western subspecies, D. variabilis roemeri Philippi, 
1849, continues from the Mississippi delta to Campeche, 
Mexico. In spite of Morrison’s revision, some authorities 


have not recognized the specific status of D. parvula 
(ABBOTT, 1974; DANCE, 1990), considering D. parvula to 
be merely an ecomorph of D. variabilis (R. T. Abbott, 
personal communication). 

As Morrison (1971) and MIKKELSEN (1985) point out, 
studies of the growth rates of Donax in the south Atlantic 
may have been complicated by the possible presence of two 
species in the samples used for analysis. Similar problems 
of interpretation exist for some early studies of tidal mi- 
gration behavior (TURNER & BELDING, 1957) and re- 
cruitment patterns (PEARSE ef al., 1942). The present paper 
presents data on the spatial distribution patterns, mor- 


Page 318 


Table 1 


Electrophoretic methods used. Allozyme abbreviations are 
explained in the text. 


Num- _ Poly- Buffer no. 
ber mor- (WERTH, 
Allozyme of loci — phic Buffer 1985) 
ACPH 1 no tris-citrate pH 8 7 
GOT 1 no tris-citrate pH 8 7 
IDH 1 no morpholine pH 6.5 1 
LAP 1 yes lithium hydroxide 3 
MDH 2 no morpholine pH 6.5 1 
ME 1 no morpholine pH 6.5 1 
6-PGD 1 yes morpholine pH 6.5 1 
GPI 1 yes tris-citrate pH 7 8 
PGM 1 yes ‘tris-citrate pH 8 7 


phometrics, and allozyme frequencies for D. variabilis and 
D. parvula from Melbourne Beach, Florida, to resolve the 
species issue. 


MATERIALS anp METHODS 


Collections of Donax were made at approximately monthly 
intervals between February 1982 and August 1983 on a 
moderately exposed sand beach at Melbourne Beach, Flor- 
ida, at Florida Department of Natural Resources coastal 
construction survey marker R-140 (28°2’55”N, 80°34’ 
54”W). Details of the sampling site and sampling methods 
are given in BONSDORFF & NELSON (1992). 

Four replicate 20.3-cm-diameter cores were taken at the 
high tide line, the base of the swash zone, and at 61 and 
91 m from the high tide line. Water depths at the 61- and 
91-m sites were in the range 1.5-3 m. All samples were 
sieved in the field on a 0.5-mm-mesh screen, fixed in 10% 
formalin, resieved on a 0.5-mm screen in the laboratory, 
and preserved. 

All Donax were identified under a dissecting microscope. 
Small individuals (<3 mm) could not always reliably be 
assigned to one species, and most were classed as Donax 
spp. 

The subsamples used for morphometric analysis were 
identified by Mr. Paul Mikkelsen, who has experience 
with these Donax species (MIKKELSEN, 1978, 1981, 1985), 
following the guidance of MORRISON (1971). Photographs 
of both species are available in MorRRISON (1971: pl. 1, 
2). Voucher specimens were deposited in the Harbor Branch 
Oceanographic Museum, Fort Pierce, Florida (D. parvula, 
Catalog Nos. HBOM 064:01965, HBOM 064:01966, 
HBOM 064:01967; D. variabilis, Catalog Nos. HBOM 
064:01968, HBOM 064:01969). 

Length, height and width of each shell were measured 
with an optical micrometer. Linear regression equations 
were computed relating shell length, height, and width 
from subsamples of both species. Data sets were checked 
for homogeneity of variances with the F.,,,-test. Analysis 


Table 2 


Regression equations relating shell measurements for Do- 
nax variabilis and D. parvula with Analysis of Covariance 
results, where appropriate. 


Comparison Equation F value (slopes) 
Width vs. length 
D. variabilis y = 0.51x — 0.42 (1) 
D. parvula y = 0.62x — 0.63 
Width vs. height 
D. variabilis y= 0091 SOK8 4.68; P < 0.05 
D. parvula y = 1.10% — 1:00 
Height vs. length 
D. variabilis y = 0.58x + 0.01 (1) 
D. parvula y = 0.53x + 0.63 


(1) Variances heterogeneous; no test possible. 


of covariance (SOKAL & ROHLF, 1981) was used to compare 
the regression equation between the two species for data 
sets with homogeneous variances. 

From the above subsamples, 20 specimens of each spe- 
cies were oriented horizontally with the left valve down, 
and the dorsal margin of the shell immediately anterior 
and posterior to the umbo was traced with the aid of a 
camera lucida. The angle between the anterior and pos- 
terior shell margins of the drawing was then measured 
with a protractor. 

On 29 April 1990 specimens of Donax variabilis and D. 
parvula were collected from the same Melbourne Beach 
study site and sorted live. The clams were placed in plastic 
vials, packed with dry ice, and transported to George Ma- 
son University for allozyme analysis. All allozymes were 
visualized using starch gel electrophoresis (WERTH, 1985). 
The enzymes examined and the buffers used are listed in 
Table 1. 


RESULTS 
Morphometric Comparisons 


The regression equations relating shell width and shell 
length, shell width and shell height, and shell height and 
shell length for both species of Donax are given in Table 
2. For width versus length and height versus length, two- 
tailed F-tests (SOKAL & ROHLF, 1981) indicated hetero- 
geneity of variances between species. Transformation did 
not resolve this problem, and therefore no analysis of co- 
variance is presented. In both cases, slopes of the regression 
lines were similar. 

The heterogeneous variances may be due to the inclusion 
of a much larger range of sizes (primarily large individ- 
uals) of Donax variabilis compared to D. parvula. The lack 
of larger D. parvula does not appear to be solely an artifact 
of the subsample. Individuals in the size range of 7-8 mm 


W. G. Nelson et al., 1993 


= Donaxparvula © Donax variabilis 


Width (mm) 
S Gi @ 


wo 


2 4 6 8 10 12 14 16 
Length (mm) 


Figure 1 


Scattergrams of shell width (mm) vs. shell length (mm) for Donax 
variabilis and D. parvula (regressions given in Table 2) illustrating 
the overlap in morphometric distributions. 


were relatively common in some months, but were not 
represented in the subsample. However, while the largest 
specimen of D. parvula collected in 16 months of sampling 
was approximately 12 mm, individuals larger than 8 mm 
were rarely recorded (BONSDORFF & NELSON, 1992). Adult 
shell size in D. parvula is truly smaller than it is in D. 
variabilis. 

Some overlap in the relationship of shell width versus 
shell length exists for Donax variabilis and D. parvula (Fig- 
ure 1). Analysis of covariance indicated that the slopes of 
the lines relating shell width and shell height for the two 
Donax species are significantly different (Table 2, Figure 
2), with width increasing more rapidly for a given height 
increase in D. parvula. Overlap of shell width and shell 
height relationships for the two species was also present. 


© Donax variabilis 


2 4 6 8 
Height (mm) 
Figure 2 


Scattergrams of shell width (mm) vs. shell height (mm) for Donax 
variabilis and D. parvula (regressions given in Table 2) illustrating 
the overlap in morphometric distributions. 


Page 319 


Table 3 
Allele frequencies for GPJ and PGM in Donax species. 


GPI allele D. variabilis (n = 101) D. parvula (n = 89) 
1 0.0099 0.0225 
2 0.0891 0.4663 
3 0.8366 0.4944 
4 0.0644 0.0169 


PGM allele D. variabilis (n = 77) Dz. parvula (n = 76) 


1 0.0519 0.0066 
2 0.7078 0.0921 
3 0.2338 0.8421 
4 0.0065 0.0592 


Measurement of the angle between the anterior and 
posterior dorsal shell margins in the vicinity of the umbo 
clearly separated the two species. The mean shell angle 
for Donax parvula was 120.9° while that for D. variabilis 
was 131.4°, a highly significant difference (t-test, t = —8.76, 
P < 0.001). There was no significant relationship of shell 
angle to total shell length for D. parvula, whereas the 
regression of these variables showed a significant positive 
relationship for D. variabilis (y = 1.02x + 119.29, t = 3.37, 
P< 0101): 


Allozyme Comparisons 


On the basis of a sample of 20 individuals per species, 
the genes for acid phosphatase (ACPH), glutamate oxa- 
loacetate transaminase (GOT), isocitrate dehydrogenase 
(IDH), malate dedydrogenase (MD/#Z), and malic enzyme 
(ME) were monomorphic and showed no differences be- 
tween the two species. Leucine aminopeptidase (LAP) and 
6-phosphogleuconate dehydrogenase (6-PGD) were defi- 
nitely polymorphic, but the resolution of their allozymes 
was poor, especially in Donax parvula, and allele frequen- 
cies were not considered to be reliable. Only the allozymes 
for phosoglucomutase (PGM) and glucose phosphateiso- 
merase (GP) were both polymorphic and easily scorable. 
These genes were examined in larger samples, and the loci 
did distinguish between the two taxa. Although all of the 
alleles were present in both species, the patterns of allele 
frequencies were clearly different. For the gene PGM, 
species differed in major allele, while for GPI, D. variabilis 
had a majority allele and D. parvula did not (Table 3). 

The differences between the two taxa for both GP/ and 
PGM were highly significant (GPI, P < 0.001; PGM, P 
< 0.001; G-test of independence, SOKAL & ROHLF, 1981). 
Within each species, genotype frequencies for each locus 
were tested for conformance to Hardy-Weinberg expec- 
tation using the chi-square statistic. Because of the large 
number of possible genotypes (10 for each locus) and the 
small expectations for some of them, all but the two most 
common genotypes (or for GPJ in Donax parvula, the three 


Page 320 


Table 4 


Spatial distribution patterns of numerical abundance of 

Donax parvula and D. variabilis at Indialantic and Mel- 

bourne Beach, Florida. Data are mean number per m? (15 

cm diameter core, n = 3) for all three study sites of SPRING 
(1981). 


Distance from the high tide line (m) 


Season 0 5 27 55 73 91 


Donax parvula 
Summer 11.3 73.4 19728 > 4011 33900 75.1 


Fall 0.0 0.0 5.6 LES) 56.5 118.6 
Winter 0.0 0.0 0.0 33.9 11.3 45.2 
Spring 0.0 0.0 33:9 169.5— 231-6 14102 


Composite 2.8 16.9 56.5 152.5 158.2 124.2 


Donax variabilis 
Summer 84.7 118.6 638.4 779.7 225.0 11.3 


Fall 790.9 73.4 90.4 113.0 84.7 101.4 
Winter 5.6 50.8 0.0 124.3 62.2 67.8 
Spring 519.8 474.6 56.5 50.8 52.5 33:9 


Composite 350.3 180.8 197.7 265.5 101.6 50.8 
Donax spp. (<3 mm) 


Summer 203.4 412.4 2740.1 2858.7 84.7 1446.3 
Fall 0.0 0.0 1446.3 5124.3 2711.4 1983.0 
Winter 0.0 0.0 45.2 870.1 502.8 1446.3 
Spring 0.0 0.0 627.1 1791.0 1101.7 113.0 


Composite 50.8 101.6 1214.6 2661.0 1096.0 1242.9 


most common), were pooled into a single class for the 
statistical test. None of the deviations from Hardy-Wein- 
berg was significant (P = 0.05). 


Spatial Distribution Patterns 


SPRING (1981) sampled three locations quarterly (in- 
cluding R-140) off Indialantic and Melbourne Beach, 
Florida, during 1979 and 1980. A detailed breakdown of 
Spring’s original data indicates some evidence of spatial 
separation of Donax variabilis and D. parvula, and of sea- 
sonal changes in the degree of separation (Table 4). During 
fall and spring, D. variabilis was relatively more abundant 
inshore and D. parvula was found in relatively greater 
abundances offshore. During the summer, maxima of both 
species were found at the same location subtidally at in- 
termediate distances from the shore (27-55 m from high 
tide line). During winter, density maxima of both species 
were found offshore (55-91 m from high tide). Small in- 
dividuals of the two species (combined for this analysis) 
tended to have a maximum density offshore at all seasons, 
with the maximum more seaward during the winter (Table 
4). At all seasons, distributions of both species were broadly 
overlapping. 

The spatial distribution patterns of the two species based 
on the more extensive collections in the present study in- 
dicate somewhat different patterns from those found in 
Spring’s collections. Donax variabilis was relatively more 


The Veliger, Vol. 36, No. 4 


Table 5 


Spatial distribution patterns of numerical abundance of 

Donax parvula and D. variabilis at Melbourne Beach, Flor- 

ida. Data are mean number per m’, with n = 3 months 

of samples for summer and fall and n = 4 and 6 for winter 
and spring, respectively. 


Distance from the high tide line (m) 


Swash 
Season 0 zone 61 91 

Donax parvula 

Summer 0.0 41.7 293.3 290.7 

Fall 0.0 259.0 397.3 124.3 

Winter 0.0 393.0 101.3 89.5 

Spring 0.0 26.0 W922 90.8 

Composite 0.7 179.9 217.8 148.8 
Donax variabilts 

Summer 0.0 85.6 757.6 163.0 

Fall 10.3 59.7 29.8 122.3 

Winter 2.0 52.9 140.3 552.6 

Spring AES 31.0 1074.3 399.6 

Composite HED 57-3 500.5 309.4 
Donax spp. (<3 mm) 

Summer Qe 5.3 2155.0 324.0 

Fall 0.0 44.6 844.0 7245.0 

Winter 0.0 0.0 115.0 387.0 

Spring 0.0 0.0 1462.0 1092.0 

Composite 0.7 11.7 6004.0 2262.0 


abundant at offshore locations (61-91 m) at all seasons 
(Table 5). Donax parvula tended to be found offshore dur- 
ing spring and summer, and tended to move inshore during 
fall and winter. The density maxima for both species were 
generally in the same subtidal region for three seasons, 
showing some separation during winter. Thus the degree 
of spatial separation shown by the two species was less 
than shown in SPRING’s (1981) data (Table 4). Small 
Donax, as Spring found, had much greater abundances at 
the offshore stations at all seasons (Table 5). 


DISCUSSION 
Morphometric and Genetic Characteristics 


According to MORRISON (1971), one of the morpholog- 
ical features for distinguishing between Donax variabilis 
and D. parvula is the relative width of shells. While sig- 
nificant difference in the regression of shell width versus 
shell height was found, that between shell width and length 
could not be statistically evaluated. Scatter plots of both 
pairs of variates (Figures 1, 2) showed that there is some 
overlap for most of the size range of the specimens ex- 
amined. This was particularly true for smaller individuals. 
The situation with regard to sympatric D. variabilis and 
D. parvula in terms of morphometric overlap of shell width 
versus length differs from a case examined by ANSELL 
(1983b) for four species of Donax occurring in Hong Kong. 


W. G. Nelson et al., 1993 


Three of four species showed no overlap for scattergrams 
of shell width versus length. One species showed total 
overlap of these parameters with a second species, but the 
species were not recorded sympatrically. 

Separation of Donax variabilis and D. parvula on the 
basis of relative shell width alone is difficult. Shell shape 
is known to be extremely variable in some Donax species 
(WADE, 1967; ANSELL, 1983a). MORRISON (1971) stated 
that “the posterior slope of D. parvula is glossy and not 
externally radially ribbed” as is the case for D. variabilis. 
However, this character also appears to be undeveloped 
for very small specimens. 

Measurement of the angle between the anterior and 
posterior dorsal margins of the shell in the vicinity of the 
umbo gave a clear separation between the two species. 
Using the photographs of the two species in MORRISON 
(1971: pl. 1, 2), measurements of shell angle gave values 
virtually identical to the mean values reported here. More 
detailed studies of the morphology of these two species, 
including soft tissues, may provide additional characters 
for accurate separation of these species in ecological studies. 
This is particularly needed for the smallest specimens, 
which may be numerically dominant in quantitative col- 
lections (BONSDORFF & NELSON, 1992). 

Genetic differences in allozymes do not definitively sep- 
arate the two species. No fixed differences between the 
two species were found among the invariant loci and no 
unique alleles were detected among the variable genes. 
However, because the two species are broadly sympatric, 
it is likely that their gene pools are separate. Differenti- 
ation in allele frequencies to the extent found in this study 
is not likely when hybridization is more than a rare oc- 
currence, but, in the absence of genetic markers unique to 
one species, the possibility cannot be excluded. 

On the bases of shell morphology and allozymic fre- 
quencies, Donax variabilis and D. parvula present a case 
intermediate among situations reported for Mytilus, Ma- 
coma, and Mercenaria. KOEHN et al. (1984) found a similar 
level of allozymic differentiation among allopatric popu- 
lations of the blue mussel Mytilus edulis, but reported no 
morphological differences. They nevertheless considered 
the differences great enough to raise a suspicion that cryp- 
tic, unrecognized species existed in the northern Atlantic. 
Because the putative species in their study were not sym- 
patric, the possibility of interbreeding could not be as- 
sessed. 

MEEHAN (1985) found little morphological differences 
among populations of Macoma balthica from the eastern 
and western Atlantic, although genetic similarity values 
between these populations were sufficiently low for them 
to be considered separate species. Differences among pop- 
ulations included both unique alleles and large differences 
in allele frequencies. 

In a comparison of the hard clams Mercenaria mercenaria 
and M. campechiensis, DILLON & MANZzI (1989) found 
comparable morphological, and greater allozymic, differ- 
entiation than reported here for Donax variabilis and D. 


Page 321 


parvula. Although they also did not report fixed differences 
in alleles for the loci examined, they did find 15 alleles 
that were unique to one or the other species. When they 
examined clams from a mixed population, they found con- 
vincing genetic and morphological evidence for hybridiza- 
tion, a situation that cannot yet be assessed in Donax. 


Spatial Distribution 


ANSELL (1983a) commented that in general, where more 
than one species of Donax occurs within an area, there is 
little habitat overlap between the species. MORRISON (1971) 
observed complete spatial separation of D. variabilis and 
D. parvula on a wide beach in South Carolina, and a high 
degree of separation has been observed for these species 
near Jacksonville Beach, Florida (the type locality for D. 
parvula), where the beach also tends to be broad with a 
low slope (P. S. Mikkelsen, personal communication). 
Morrison (1971) described D. variabilis as living inter- 
tidally throughout the year, with part of the population 
often remaining in mid-intertidal areas during low tide. 

Complete spatial separation of Donax variabilis and D. 
parvula does not invariably occur. LEBER (1982) found 
that on the coast of North Carolina these species migrated 
together in the swash zone from January through July. 
In August, D. parvula disappeared from the intertidal zone 
and Leber suggested that it had migrated seaward to 1 m 
depth in the surf zone. Donax variabilis ceased tidal mi- 
grations in August and remained high on the beach in 
damp sand. Both species had disappeared from the inter- 
tidal by December, and recolonized the beach in the fol- 
lowing March. Leber did not regularly sample the subtidal 
area, and thus what may have occurred subtidally is un- 
clear. 

At Melbourne Beach, which has a fairly steep slope and 
high energy, there was never a clear spatial separation of 
the two species. These collections do not support 
MorrRISON’s (1971) suggestion that Donax variabilis is 
mainly an upper intertidal species. Both D. variabilis and 
D. parvula were maximally abundant at the offshore, sub- 
tidal locations at the Melbourne Beach site. MATTA’S (1977) 
work in North Carolina, in an area believed to be north 
of the distributional limit of D. parvula, recorded Donax 
spp. (presumably D. variabilis or possibly D. fossor) as 
concentrated all year subtidally at 30-60 m distance from 
the high tide line. Distribution of small individuals was 
similar to that found in the present study. 

Local differences in abundance along a beach gradient 
may be affected not only by the tides (TURNER & BELDING, 
1957) and seasons (LEBER, 1982), but also by beach mor- 
phology (DONN et al., 1986). Local differences in organic 
input to beaches have also been shown to influence pop- 
ulation characteristics of a Donax species (SASTRE, 1984). 
Therefore, it may be found that the spatial distribution 
patterns of D. variabilis and D. parvula may be variable 
from site to site. 

The distribution pattern of two species from the Texas 


Page 322 


The Veliger, Vol. 36, No. 4 


coast, Donax variabilis roemeri and D. texasianus Philippi, 
1847, showed similarities to the situation in North Car- 
olina in that complete spatial separation occurred at some, 
but not all, times of the year (VEGA & TUNNELL, 1987). 
Donax v. roemeri occurred intertidally and D. texasianus 
occurred subtidally from February until April. At least a 
portion of the population of both species migrated tidally 
during May to August. 

With the exceptions of the present study and of MATTA’s 
(1977) work from North Carolina, the majority of studies 
of Donax on the Atlantic coast have almost exclusively 
sampled in the intertidal zone (e.g., MIKKELSEN, 1981; 
LEBER, 1982; ADAMKEWICZ, 1989). On the central Florida 
coast, a substantial portion of both D. variabilis (93%) and 
D. parvula (67%) were found subtidally, even when in- 
dividuals were also present in the intertidal (BONSDORFF 
& NELSON, 1992). For individuals <3 mm in length, 99.9% 
of all Donax were found subtidally. In Texas, VEGA & 
‘TUNNELL (1987) showed that 15% of Donax. v. roemeri 
and 85% of D. texasianus were found subtidally. Failure 
to account for the subtidal portion of the population in 
studies of Donax will clearly lead to a highly biased de- 
scription of population characteristics. 


ACKNOWLEDGMENTS 


Financial support for the collection of samples was pro- 
vided by the Florida Sea Grant College program with 
support from the National Oceanic and Atmospheric Ad- 
ministration, Office of Sea Grant, U.S. Dept. of Commerce, 
Grant No. NA80AA-0-0038 to WGN. Additional support 
was received from the Abo Akademi Research Foundation 
(WGN), and the U.S. Educational Foundation in Finland, 
the Academy of Finland, and the Maj and Tor Nessling 
Foundation in Finland (EB). T. Allenbaugh and D. Peters 
assisted in sample collection. The provision of original 
Donax data from the Melbourne area by K. D. Spring is 
greatly appreciated. The assistance of Mr. Paul Mikkelsen 
in distinguishing between the two Donax species was es- 
sential to the paper. 


LITERATURE CITED 


ABBOTT, R. T. 1974. American Seashells. 2nd. ed. Van Nos- 
trand Reinhold: New York. 663 pp. 

ADAMKEWICZ, L. 1989. Differences in the frequencies of several 
shell characteristics in the clam Donax variabilis around Cape 
Hatteras, North Carolina. The Veliger 32:21-28. 

ANSELL, A. D. 1983a. The biology of the genus Donax. Pp. 
607-635. In: A. McLachlan & T. Erasmus (eds.), Sandy 
Beaches as Ecosystems. Dr. W. Junk Publishers: The Hague. 

ANSELL, A. D. 1983b. Species of Donax from Hong Kong: 
morphology, distribution, behaviour, and metabolism. Pp. 
19-47. In: B. Morton & D. Dudgeon (eds.), Proceedings of 
the Second International Workshop on the Malacofauna of 
Hong Kong and Southern China. Hong Kong University 
Press: Hong Kong. 

30NSDORFF, E. & W.G. NELSON. 1992. Some observations on 
the ecology of the coquina clams Donax variabilis Say, 1822, 


and Donax parvula Philippi, 1849, on the east coast of Florida. 
The Veliger 35:358-365. 

DANCE, P. S. (ed.) 1990. The Collectors Encyclopedia of Shells. 
Zachary Kwintner Books Ltd.: London. 288 pp. 

DILLon, R. T. & J. J. MANzI. 1989. Genetics and shell mor- 
phology in a hybrid zone between the hard clams Mercenaria 
mercenaria and M. campechiensis. Marine Biology 100:217- 
222. 

Donn, T. E., JR., D. J. CLARKE, A. MCLACHLAN & P. Du Tor. 
1986. Distribution and abundance of Donax serra Roding 
(Bivalvia: Donacidae) as related to beach morphology. I. 
Semilunar migrations. Journal of Experimental Marine Bi- 
ology and Ecology 102:121-131. 

KoEnN, R. K., J. G. HALL, D. J. INNES & A. J. ZERA. 1984. 
Genetic differentiation of Mytilus edulis in eastern North 
America. Marine Biology 79:117-126. 

LEBER, K. M. 1982. Bivalves (Tellinacea: Donacidae) on a 
North Carolina beach: contrasting population size structures 
and tidal migrations. Marine Ecology Progress Series 7:297- 
301. 

Matta, J. F. 1977. Beach fauna study of the CERC field 
research facility, Duck, North Carolina.—U.S. Army Corps 
of Engineers, Coastal Engineering Research Center, Misc. 
Report 77-6. 

MEEHAN, B. W. 1985. Genetic comparison of Macoma balthica 
(Bivalvia, Tellinidae) from the eastern and western North 
Atlantic Ocean. Marine Ecology Progress Series 22:69-76. 

MIKKLESEN, P.S. 1978. A comparison of intertidal distribution, 
growth rates and shell polychromism between two Florida 
populations of the coquina clam, Donax variabilis Say, 1822 
(Bivalvia: Donacidae). M.S. Thesis, Florida Institute of 
Technology, Melbourne, Florida. 78 pp. 

MIKKELSEN, P. S. 1981. A comparison of two Florida popu- 
lations of the coquina clam, Donax variabilis Say, 1822 (Bi- 
valvia: Donacidae). I. Intertidal density, distribution, and 
migration. The Veliger 23:230-239. 

MIKKELSEN, P. S. 1985. A comparison of two Florida popu- 
lations of the coquina clam, Donax variabilis Say, 1822 (Bi- 
valvia: Donacidae). II. Growth rates. The Veliger 27:308- 
311. 

Morrison, J. P. E. 1971. Western Atlantic Donax. Proceedings 
of the Biological Society of Washington 83:545-568. 

PEARSE, A.S.,H. J. HUMM & G.W. WuHarRTON. 1942. Ecology 
of sand beaches at Beaufort, North Carolina. Ecological 
Monographs 12:136-190. 

SASTRE, M. P. 1984. Relationships between environmental 
factors and Donax denticulatus populations in Puerto Rico. 
Estuarine Coastal and Shelf Science 19:217-230. 

SPRING, K. D. 1981. A study of the spatial and temporal vari- 
ation in the nearshore macrobenthic populations of the cen- 
tral Florida east coast. M.S. Thesis, Florida Institute of 
Technology, Melbourne, Florida. 67 pp. 

SOKAL, R.R. & F. J. ROHLF. 1981. Biometry. W. H. Freeman: 
San Francisco. 859 pp. 

TURNER, H. J., JR. & D. L. BELDING. 1957. The tidal mi- 
grations of Donax variabilis Say. Limnology and Oceanog- 
raphy 2:120-124. 

VEGA, R.R. & J. W. TUNNELL, JR. 1987. Seasonal abundance, 
zonation, and migratory behavior of Donax (Donacidae: Bi- 
valvia) on Mustang and Northern Padre Island, Texas. Mal- 
acology Data Net (Ecosearch Series) 1:97-136. 

WaDE, B. A. 1967. On the taxonomy, morphology, and ecology 
of the beach clam, Donax striatus Linne. Bulletin of Marine 
Science 17:723-740. 

WERTH, C. R. 1985. Implementing an isozyme laboratory at 
a field station. Virginia Journal of Science 36:53-76. 


The Veliger 36(4):323-331 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


New Reports of the Large Gastropod Campanile 


from the Paleocene and Eocene of the 


Pacific Coast of North America 


by 


RICHARD L. SQUIRES 


Department of Geological Sciences, California State University, 
Northridge, California 91330, USA 


Abstract. 


The Old World Tethyan prosobranch gastropod genus Campanile Fischer, 1884, is reported 


from six new localities in California. Three of these new reports are for the late Paleocene C. greenellum 
Hanna & Hertlein, 1939, with two localities in the Santa Susana Formation, Santa Monica Mountains, 
southern California, and a locality in the San Francisquito Formation, Redrock Mountain area near 
Castaic Lake, southern California. These are the first reports of C. greenellum from southern California. 
The three other new reports are for the early Eocene C. dillont Hanna & Hertlein, 1949, with localities 
in both the Santa Susana and Llajas Formations, Bus Canyon, south side of Simi Valley, southern 
California, and a locality in the Sierra Blanca Limestone near Oso Canyon, Santa Ynez River Valley, 
southern California. 

A previously known Paleocene Campanile sp. in an unnamed mudstone in the northern Santa Lucia 
Range, central coastal California, is herein identified as Campanile sp. indet. Campanile sp. Nelson, 
1925, from the Sierra Blanca Limestone near Lake Cachuma, southern California, is herein identified 


as C. dilloni. 


INTRODUCTION 


The gastropod genus Campanile Fischer, 1884, has a geo- 
logic range from Late Cretaceous (Maastrichtian) to Re- 
cent (WENZ, 1940). The genus is best known from the 
Paris Basin Eocene fauna where well-preserved specimens 
of C. giganteum (Lamarck, 1804), up to a meter in length, 
are known from middle Eocene (Lutetian) strata of Dame- 
ry near Epernay, France. These specimens, and some of 
about the same size from Jamaica (JUNG, 1987), are among 
the largest gastropods of all time. 

During the early Tertiary, Campanile underwent a geo- 
graphic expansion. Many species lived in the Old World 
Tethys Sea, but some migrated westward. The distribution 
of known occurrences of early Tertiary Campanile extends 
in a band from northwest India through France, to Ala- 
bama and the Caribbean area, and on into Baja California 
Sur, Mexico, and California. Campanile was an Old World 
Tethyan genus that immigrated into North America dur- 
ing the Paleogene (GIVENS, 1989). Campanile arrived in 
California during the Paleocene (SQUIRES, 1984). Only a 
single species, C. greenellum Hanna & Hertlein, 1939, is 
known, and it has been found at a few localities in northern 


California. It is characterized by a wide pleural angle 
(approximately 35°), numerous wide nodes (approximate- 
ly 22) on the carina in the posterior part of the whorls, 
and three spiral ribs anterior to the carina. I report here 
three new localities for this rare species from upper Pa- 
leocene strata in southern California. 

During the early Eocene, which was the warmest time 
of the Cenozoic (HAQ, 1981), Campanile attained its max- 
imum geographic distribution for the Pacific coast region 
of North America. Only a single species, C. diliont Hanna 
& Hertlein, 1949, is known, and it has been found at 
several localities from southern to south-central California. 
It is characterized by a relatively narrow pleural angle 
(approximately 20°), approximately 8 to 16 nodes on the 
carina in the posterior part of the whorls, and three to 
four spiral ribs anterior to the carina. I report here three 
new localities for this rare species from lower Eocene strata 
in southern California. 

By middle Eocene time, Campanile disappeared from 
the Pacific coast region of North America. On a worldwide 
basis, after the middle Eocene, there was a sharp decrease 
in the species diversity of Campanile. Neogene and Pleis- 


Page 324 


115° 


California 
™ PREVIOUS LOCALITIES 


A NEW LOCALITIES 


@ A Paleocene Campanile 
sp. indet. 


@ Unnamed 
mudstone 


San 
Francisquito 


Figure 1 


Index map of previous and new localities of Campanile greenellum 
Hanna & Hertlein, 1939. 


tocene records are scarce, and the sole surviving species is 
C. symbolicum Iredale, 1917, which lives in large popu- 
lations on sandy patches between rocks in depths of 1 to 
4 m along the southwestern coast of Australia (HOUBRICK, 
1984). 

The term “Martinez Stage” used in this report has had 
a complex nomenclatural history and a variable geologic 
age assignment since first introduced as a concept by early 
workers in the 1860s (CLARK & VOKES, 1936). Workers 
now assign this provincial stage to the late Paleocene (SAUL, 
1983a:fig. 1; ZINSMEISTER, 1983). The terms ““Meganos 
Stage” and “‘Capay Stage” used in this report stem from 
CLARK & VOKES (1936), who informally proposed Pacific 
coast of North America provincial megainvertebrate Eo- 
cene stages. The ““Meganos Stage” has been refined by 
SAUL (1983a) to be latest Paleocene to early Eocene in 
age, and the ““Capay Stage” has been refined by GIVENS 
(1974) to be restricted to the middle early Eocene. These 
refinements are summarized in SQUIRES (1988) and are 
used here. 

Abbreviations used for catalog and/or locality numbers 
are: CAS, California Academy of Sciences, San Francisco; 
CSUN, California State University, Northridge; LAC- 
MIP, Natural History Museum of Los Angeles County, 


The Veliger, Vol. 36, No. 4 


1152 


California 
™@ PREVIOUS LOCALITIES 


A NEW LOCALITIES 


Sierra Blanca 
Limestone 


ro) 
200km << 


ss ape Wy 


Figure 2 


Index map of previous and new localities of Campanile dillon 
Hanna & Hertlein, 1949. 


Invertebrate Paleontology Section; LSJU, Leland Stan- 
ford, Jr., University (collections now housed at the CAS); 
UCLA, University of California, Los Angeles (collections 
now housed at the LACMIP); UCMP, University of Cal- 
ifornia Museum of Paleontology, Berkeley. 


NEW LOCALITIES oF 


Campanile greenellum 


The three new localities of Campanile greenellum are from 
the Los Angeles area, southern California (Figure 1). Two 
of the localities are from Trailer Canyon in the Santa 
Monica Mountains at LACMIP locs. 24433 and 27023. 
DIBBLEE (1992) mapped the rocks in the area of the lo- 
calities as the Santa Susana Formation of Paleocene age. 
The only fossil found at locality 24433 was a single spec- 
imen of C. greenellum (Figure 3). It is a well-preserved 
7.5-cm-long fragment. The specimen was found in a very 
fine-grained silty sandstone, rich in fragments of calcareous 
algae. The only fossil at nearby locality 17023 was a single 
specimen of C. greenellum (Figure 4). It is an internal mold 
of a 4.5-cm-long fragment of the upper spire, and it shows 
the diagnostic numerous whorl-shoulder nodes. The spec- 
imen was found in micaceous sandstone. 


R. L. Squires, 1993 


Page 325 


Explanation of Figures 3 to 5 


Figures 3-5. Campanile greenellum Hanna & Hertlein, 1939. Figure 3. Hypotype LACMIP 12232, LACMIP loc. 
24433, Santa Susana Formation, Santa Monica Mountains, abapertural? view, 0.89. Figure 4. Hypotype LAC- 
MIP 12233, LACMIP loc. 27023, Santa Susana Formation, Santa Monica Mountains, apertural view, x 1.36. 
Figure 5. Hypotype LACMIP 12234, LACMIP loc. 24716, lower San Francisquito Formation, Redrock Mountain, 


internal mold, abapertural? view, x 0.70. 


The third new locality of Campanile greenellum is from 
the lower part of the San Francisquito Formation on Red- 
rock Mountain, near Castaic Lake, at LACMIP loc. 24716. 
SAUL (1983b:94, 124) assigned the age of the rocks at this 
locality to the late Paleocene on the basis of the presence 
of Turritella peninsularis Anderson & Hanna, 1935. Ac- 
cording to Saul (personal communication), the specimens 
of 7. peninsularis at this locality are very close in mor- 
phology to 7. peninsularis quayle: Saul, 1983b, of early 
Paleocene age. At LACMIP loc. 24716, three internal 
molds of C. greenellum were found. The largest specimen 
(Figure 5) shows best the diagnostic wide pleural angle 
and the numerous whorl-shoulder nodes. The specimens 
were found in coarse-grained sandstone and were associ- 
ated with numerous specimens of 7. peninsularis, a few 
ostreid fragments, and a few other gastropod internal molds. 


NEW LOCALITIES or 
Campanile dilloni 


The three new localities of Campanile dilloni are from 
southern California (Figure 2), with two of the localities 
in Bus Canyon, Ventura County, and the other locality 
near Oso Canyon, Santa Barbara County. 

One of the new localities of Campanile dilloni in Bus 
Canyon is from the uppermost Santa Susana Formation 
as CSUN loc. 1565. SQuiIREs (1991a) assigned the age of 
the rocks from the same part of the Santa Susana For- 
mation (e.g., the upper 100 m) just east of loc. 1565 to the 
earliest Eocene (““Meganos Stage”). The only fossil found 


at loc. 1565 was the single specimen of C. dilloni. It is a 
well-preserved specimen (Figures 6, 7) found in steel-gray 
siltstone. 

The other new occurrence of Campanile dilloni in Bus 
Canyon is from the lowermost marine part of the Llajas 
Formation at CSUN loc. 703. The Llajas Formation un- 
conformably overlies the Santa Susana Formation. SQUIRES 
(1984) assigned the age of the Llajas Formation strata at 
locality 703 to the middle early Eocene (“Capay Stage’’). 
Although numerous shallow-marine macrofossils were 
found at this locality, only a single specimen (Figure 8) 
of C. dillonit was found. It is an internal mold, but it is of 
large size and has a narrow pleural angle. Both of these 
features help to distinguish this species. 

The third new locality of Campanile dilloni is from the 
Sierra Blanca Limestone in the Oso Canyon area, Santa 
Ynez River Valley, at CSUN loc. 1566. DIBBLEE (1987) 
assigned the age of the Sierra Blanca Limestone in this 
area to the early Eocene. Only a single specimen (Figures 
9, 10) of C. dilloni was found there. It is an internal mold 
of large size with a narrow pleural angle. 


SYSTEMATIC PALEONTOLOGY 
Family CAMPANILIDAE Douville, 1904 
Genus Campanile Fischer, 1884 


Type species: Cerithium giganteum Lamarck, 1804, by 
subsequent designation, Sacco, 1895; Eocene, Paris Basin, 
France. 


Explanation of Figures 6 to 11 


Figures 6-11. Campanile dilloni Hanna & Hertlein, 1949. Figures 6, 7. Hypotype LACMIP 12235, CSUN loc. 
1565, upper Santa Susana Formation, Bus Canyon, Simi Valley, x0.59. Figure 6. Apertural view. Figure 7. 
Abapertural view. Figure 8. Hypotype LACMIP 12236, CSUN loc. 703, Llajas Formation, Bus Canyon, Simi 
Valley, internal mold, abapertural view, x0.52. Figures 9, 10. Hypotype LACMIP 12237, CSUN loc. 1566, Sierra 
Blanca Limestone, near Oso Canyon, Santa Barbara County, internal mold, x0.49. Figure 9. Apertural view. 
Figure 10. Abapertural view. Figure 11. Hypotype LACMIP 12238, CSUN loc. 955 = UCMP loc. A-2990, Sierra 
Blanca Limestone, Lazaro Creek, Santa Barbara County, internal mold, abapertural view, <0.47. 


R. L. Squires, 1993 


Remarks: The type species of Campanile has been much 
debated, and the reader is referred to HOUBRICK (1981) 
and SQUIRES & ADVOCATE (1986) for discussions of the 
difficulties. 

The name Campanile was used on the Pacific coast of 
North America until HANNA & HERTLEIN (1949) used 
Campanilopa Iredale, 1917. WENZz (1940) and HousBRIck 
(1981) have pointed out, however, that Campanilopa is a 
junior synonym of Campanile. 

Recent studies (HOUBRICK, 1989) on the anatomy of the 
extant Campanile symbolicum indicate that members of 
Campanilidae should no longer be considered as cerithioi- 
dean gastropods. He argued for a new systematic place- 
ment of Campanile at the base of, but outside, the ceri- 
thioidean clade. In addition, he suggested elevating the 
family Campanilidae to superfamilial status (as superfam- 
ily Campaniloidea Douvillé, 1904). PONDER & WAREN 
(1988) and Housrick (1989) rejected HASZPRUNAR’S 
(1988) idea that Campanile is in any way related to het- 
erobranch gastropods. 


Campanile greenellum Hanna & Hertlein, 1939 
(Figures 3—5) 


Campanile greenellum HANNA & HERTLEIN, 1939:101-102, 
fig. 1; KEEN & BENTSON, 1944:137. 


Original description: “Shell elongate conic, imperfect but 
with about 8 whorls. The top of each whorl ornamented 
by a band of elevated nodes, there being about 22 on the 
last whorl; below each band of nodes there are three re- 
volving cords separated from each other and from the no- 
dose band above and below by incised lines. Length (in- 
complete) approximately 95 mm, greatest width 64 mm” 
(HANNA & HERTLEIN, 1939:101). 


Type material and type locality: Holotype CAS 7233, 
near Devils Slide along California State Highway 1, south 
of San Francisco, San Mateo County, northern California. 


Geographic distribution: Santa Monica Mountains, Los 
Angeles County, southern California (herein) to Stewarts 
Point, Sonoma County, northern California. 


Stratigraphic distribution: “Martinez Stage” (upper Pa- 
leocene): Santa Susana Formation, Santa Monica Moun- 
tains, southern California (herein, LACMIP locs. 24433 
and 27023); lower San Francisquito Formation, Redrock 
Mountain, southern California (herein, LACMIP loc. 
24716); unnamed strata near Devils Slide along California 
State Highway 1, south of San Francisco, northern Cal- 
ifornia (HANNA & HERTLEIN, 1939); German Rancho 
formation (informal), northern California (WENTWORTH, 
1966, 1968). 


Remarks: The mudstone and siltstone rocks at the type 
locality of Campanile greenellum near Devils Slide are un- 
named and have been referred to (MORGAN, 1981) as 
Paleocene turbidites. 


Page 327 


WENTWORTH (1966, 1968) reported a specimen of Cam- 
panile greenellum from the Paleocene part of the infor- 
mation German Rancho formation, west of the San An- 
dreas fault, 2 km south of the town of Stewarts Point, 
northern California. The specimen, which was identified 
by W. O. Addicott, was found near the base of a sea cliff 
at Wentworth’s field loc. 730 in a bed of pebble conglom- 
erate with a matrix of very poorly sorted clayey sandstone 
(WENTWORTH, 1966:181). My attempts to find this spec- 
imen were unsuccessful. Macrofossils, which are sparse in 
the German Rancho formation, underwent post-mortem 
transport by means of turbidity currents into a deep-water 
environment, and the rocks containing the Campanile spec- 
imen have undergone right slip of at least 435 km (270 
miles) along the San Andreas fault (WENTWORTH, 1968). 
The German Rancho formation Campanile specimen, 
therefore, orginally lived in the vicinity of the southeastern 
Diablo Range or the Temblor Range, south-central Cal- 
ifornia. The northern limit of the original distribution of 
C. greenellum along the Pacific coast of North America 
during the Paleocene, therefore, was approximately the 
same as that for the Eocene-age C. dillon. 

SEIDERS & JOYCE (1984:table 1) found a specimen of 
?Campaniliopa [sic] n. sp. from an unnamed mudstone unit 
at LACMIP loc. 27203 in the northern Santa Lucia Range, 
central California coastal area. The specimen was asso- 
ciated with a few other mollusks and some brachiopods. 
The Campanile specimen and its associated fauna are stored 
at LACMIP. SEIDERS & JOYCE (1984) assigned a tentative 
late Paleocene age to the fossils. I examined the Campanile 
specimen from loc. 27203 and found it to be a deeply 
weathered fragment of an internal mold that shows only 
a small part of the body whorl. The specimen can be 
identified only as Campanile sp. indet. 


Campanile dilloni (Hanna & Hertlein, 1949) 
(Figures 6-11) 


Campanilopa dillont HANNA & HERTLEIN, 1949:393, pl. 77, 
figs. 2, 4, text-fig. 1; GIVENS, 1974:69, pl. 7, fig. 10; 
SQUIRES & ADVOCATE, 1986:853, 855, fig. 2.1. 

Campanile dilloni Hanna & Hertlein: SQUIRES, 1991b:pl. 1, 
fig. 18. 


Original description: “Shell elongate, 4 whorls present 
(shell incomplete on type); whorls rather flat-sided but 
slightly concave; top of each whorl sculptured with a pro- 
jecting carina which bears about 14 to 16 pointed nodes, 
the sides of the whorls are ornamented by about a half 
dozen spiral lirae. Paratypes in longitudinal section reveal 
the presence internally of two strong plaits on the columella 
and a rounded ridge on both the top and bottom of the 
cavity. Dimensions of holotype: height (incomplete), 72.5 
mm; diameter, 44.0 mm. Some specimens, poorly pre- 
served, indicate a height of approximately 300 mm”(HANNA 
& HERTLEIN, 1949:393). 

SQUIRES & ADVOCATE (1986:853) gave a supplementary 
description: “Turreted-elongate shell of very large size; 


Page 328 


protoconch and upper spire missing; whorls slightly con- 
cave, becoming flat sided in later whorls; posterior portion 
of each whorl with a very projecting, greatly thickened 
carina with eight to ten pointed nodes, sides of whorls with 
three to four swollen spiral cords; groove along inside of 
carina in later whorls; outer lip missing and aperture ob- 
scured by matrix.” 


Type material and type locality: Holotype CAS 9425 
and paratypes CAS 9428 and 9429, all from CAS loc. 
30667; Mabury Formation, Agua Media Creek, ‘Temblor 
Range, Kern County, south-central California. 


Geographic distribution: Orocopia Mountains, Riverside 
County, southern California, to Agua Media Creek, Tem- 
blor Range, Kern County, south-central California. 


Stratigraphic distribution: California ‘““Meganos Stage” 
(uppermost Paleocene to lower lower Eocene) to “Capay 
Stage” (middle lower Eocene). ““MEGANOS STAGE”: Up- 
permost Santa Susana Formation, Bus Canyon, south side 
of Simi Valley, Ventura County, southern California 
(herein, CSUN loc. 1565). ““CAPAY STAGE”: Lower Man- 
iobra Formation, Orocopia Mountains, Riverside County, 
southern California (SQUIRES & ADVOCATE, 1986; SQUIRES, 
1991b); lower Llajas Formation, Bus Canyon, south side 
of Simi Valley, Ventura County, southern California 
(herein, CSUN loc. 703); lower Juncal Formation, Sespe 
Hot Springs, Ventura County, southern California 
(GIVENS, 1974); Mabury Formation, Agua Media Creek, 
Temblor Range, Kern County, south-central California 
(HANNA & HERTLEIN, 1949). LOWER EOCENE (no differ- 
entiation as to stage): Sierra Blanca Limestone, near Oso 
Canyon, Santa Ynez River Valley, Santa Barbara County, 
southern California (herein, CSUN loc. 1566); Sierra 
Blanca Limestone, Lazaro Canyon, near Lake Cachuma, 
Santa Barbara County, southern California (NELSON, 1925; 
herein, CSUN loc. 955 = UCMP loc. A-2990). 


Remarks: HANNA & HERTLEIN (1949) reported that the 
type locality (CAS loc. 30667) of Campanile dilloni ex- 
tended along the outcrop for a distance of approximately 
0.8 km. In 1992, I visited the type locality and found 
outcrops to be only moderately well exposed and consisting 
of a relatively thin section of conglomeratic sandstone that 
grades upward into very fine sandstone. I found macro- 
fossils only in one small area that is equivalent to the 
middle of their reported band of outcrop. Very sparse 
macrofossil fragments of colonial corals and a few naticid 
gastropods were found in the basal sandstone. These frag- 
mentary fossils have undergone considerable post-mortem 
transport. No new specimens of C. dilloni were found. 
Overlying and underlying the sandstone are thick sequenc- 
es of mudstones. MALLORY (1970) interpreted the mud- 
stones as bathyal deposits and the intervening sandstone 
(his middle member of the Lodo Formation) as a littoral 
deposit. ALMGREN e/ al. (1988) referred to the intervening 
sandstone as the Mabury Formation, and on the basis of 


The Veliger, Vol. 36, No. 4 


calcareous nannofossil biostratigraphy, assigned an age 
that is equivalent to the “Capay Stage.” 

NELSON (1925:348) reported numerous casts of Cam- 
panile sp., some of which, if unbroken, would be over 40 
cm in length, from white limestone near Lake Cachuma, 
along Cachuma Creek, Santa Barbara County, southern 
California. He did not mention a specific locality, nor did 
he mention whether or not any specimens were stored at 
UCMP (the institution he was affiliated with). While go- 
ing through the UCMP collections, I came across several 
large, poorly preserved casts of Campanile from UCMP 
loc. A-2990 (Cachuma Creek area). According to locality 
records at UCMP, this locality is the same as UCMP loc. 
4124. KEENAN (1932:79, fig. 1) noted that UCMP loc. 
4124 is the same as LSJU locality 1106 (in the Sierra 
Blanca Limestone). The specimens from UCMP loc. 
A-2990 = LSJU 1106, therefore, must be the ones that 
NELSON (1925) reported. Unfortunately, the exact location 
of this locality is not available in the register of localities 
at UCMP. The description given in these records mentions 
only nearness to Cachuma Creek. The description given 
by KEENAN (1932:79) mentions the “east fork of Cachuma 
Creek” but also mentions a longitude and latitude that are 
equivalent to the Pacific Ocean off the coast of Baja Cal- 
ifornia. On an index map in KEENAN (1932:fig. 1), how- 
ever, LSJU loc. 1106 is shown to be on a prominent east 
fork of Cachuma Creek. 

I visited the area of UCMP loc. A-2990 and found four 
large, poorly preserved internal molds of Campanile at 
CSUN loc. 955 along the west side of Lazaro Creek, which 
is a prominent east fork of Cachuma Creek. Locality 955, 
which must be the same as UCMP loc. A-2990, coincides 
with the easternmost exposure of a thin band of Sierra 
Blanca Limestone on DIBBLEE’s (1966:pl. 3) geologic map 
of the area. On this map, the thin band of outcrop is labelled 
“Tsb” for the Sierra Blanca Limestone, but the graphic 
pattern on the map corresponds to the Pliocene Careaga 
Sandstone. The specimens at CSUN loc. 955 have the 
diagnostic narrow pleural angle and large shell size of C. 
dilloni, and they are virtually identical to the specimen 
(Figure 8) of C. dilloni from the lower Llajas Formation 
and the specimen (Figures 9, 10) of C. dillon: from the 
Sierra Blanca Limestone near Oso Canyon. Because the 
campanilid from CSUN loc. 955 has never been illustrated 
before, the best preserved specimen is shown in Figure 11. 

Campanile n. sp.? SQUIRES (1987:31-32, figs. 32, 33) 
from the lower Juncal Formation (‘““Capay Stage’’) in the 
Whitaker Peak area, Los Angeles County, southern Cal- 
ifornia, may be C. dilloni but poor preservation prevents 
a positive identification. 

SQuirRES & DEMETRION (1992:28, fig. 65) reported a 
specimen of Campanile sp. from the lower Eocene (““Capay 
Stage”) part of the Bateque Formation, Baja California 
Sur, Mexico, but the specimen is so poorly preserved that 
no species identification is possible. SQUIRES (1992) re- 
ported Campanile sp. from the ““Capay Stage” part of the 


R. L. Squires, 1993 


Tepetate Formation, Baja California Sur, Mexico, but 
poor preservation prevents species identification. 


ACKNOWLEDGMENTS 


Antony J. Marro (CSUN) collected and donated the spec- 
imen of Campanile dilloni from the upper Santa Susana 
Formation. Fen Yan (CSUN) collected and donated the 
specimen of C. dillon: from the Sierra Blanca Limestone 
in Oso Canyon. Michael P. Gring (CSUN) obtained per- 
mission for access to private property (type section of C. 
dillont). Michael P. Gring and Martin Jackson (CSUN) 
and Lindsey T. Groves (Natural History Museum of Los 
Angeles County, Malacology Section) helped in field work. 
Carl Twisselman (Buttonwillow, California) kindly al- 
lowed access to private property (type section of C. dillonz. 
Carl M. Wentworth (U.S. Geological Survey, Menlo Park) 
provided locality information, and he and Chuck Powell, 
Jr., (U.S. Geological Survey, Menlo Park) tried to find 
the specimen of Campanile greenellum from the German 
Rancho formation. LouElla Saul (LACMIP) allowed ac- 
cess to collections, provided casts of the primary type ma- 
terial of C. greenellum and C. dilloni, and shared her know]l- 
edge about new Paleocene occurrences of Campanile in 
California. She and an anonymous reviewer critically read 
the manuscript. 


LOCALITIES CITED 


CAS loc. 30667. “SW corner of sect. 27, T28S, R19E, 
through the NE % of the SE % of section 28, T28S, 
R19E, south side of headwaters of Media Agua Creek, 
Kern County, California” (HANNA & HERTLEIN, 1949: 
393). A visit by the author resulted in the following 
refinement of this description: at elevation 2650 ft. (800 
m) on a lowly resistant ridge formed by conglomeratic 
sandstone along the crest of the north side of Media 
Agua Creek, 442 m (1450 ft.) N and 183 m (600 ft.) 
E of SW corner of section 27, T28S, R19E, U.S. Geo- 
logical Survey, 7.5-minute, Las Yeguas Ranch Quad- 
rangle, 1959, Temblor Range, Kern County, south-cen- 
tral California. Mabury Formation. Age: Middle early 
Eocene (“Capay Stage”). Collectors: Earl Dillon and 
R. L. Hewitt, 1940s?. 

CSUN loc. 703. At elevation of 1430 ft. (420 m) along a 
ridge on east side of Bus Canyon, S side of Simi Valley, 
238 m (780 ft.) S and 177 m (580 ft.) W of NE corner 
of section 28, T2N, R18W, U.S. Geological Survey, 
7.5-minute, Thousand Oaks Quadrangle, 1950 (pho- 
torevised 1967), Ventura County, southern California. 
Lower Llajas Formation, lowermost part of shallow- 
marine (transgressive) facies of SQUIRES (1984). Age: 
Middle early Eocene (“‘Capay Stage’’). Collector: R. L. 
Squires, October 1988. 

CSUN loc. 955. At elevation of 2160 ft. (650 m), just 
below top of resistant hill formed by a 20-m-thick gray 
algal limestone along the west side of Lazaro Canyon, 


Page 329 


533 m (1750 ft.) S and 91 m (300 ft.) W of the SE 
corner of section 23, T7N, R29W, U.S. Geological Sur- 
vey, 7.5-minute, Figueroa Mtn. Quadrangle, 1959, Santa 
Barbara County, southern California. Sierra Blanca 
Limestone. Age: Early Eocene. Collectors: R. L. Squires 
and L. T. Groves, October 1985. Same as UCMP loc. 
A-2990, see below. 

CSUN loc. 1565. At elevation of 1100 ft. (340 m), along 
west side of Bus Canyon, S side of Simi Valley, on north 
bank of an unnamed tributary that enters Bus Canyon 
from the W, 274 m (900 ft.) S and 503 m (1650 ft.) W 
of NE corner of section 28, T2N, R18W, U.S. Geolog- 
ical Survey, 7.5-minute, Thousand Oaks Quadrangle, 
1950 (photorevised 1967), Ventura County, southern 
California. Uppermost Santa Susana Formation. Age: 
Latest Paleocene or early early Eocene (“Meganos 
Stage’’). Collector: A. J. Marro, 1985. 

CSUN loc. 1566. At elevation of 1919 ft. (600 m), ap- 
proximately 1.15 km E of Oso Canyon, on hillside on 
north side of Santa Ynez River, 175 m (575 ft.) E and 
191 m (625 ft.) S of NW corner of section 6, T5N, 
R27W, U.S. Geological Survey, 7.5-minute, San Mar- 
cos Pass Quadrangle, 7.5 minute, 1959 (photorevised 
1988), Santa Barbara County, southern Caifornia. Si- 
erra Blanca Limestone. Age: Early Eocene. Collector: 
F. Yan, 1986. 

LACMIP 24433. 150 m (500 ft.) NE of the end of the 
entry road to quarry in Trailer Canyon, stratigraphi- 
cally just below white algal limestone, U.S. Geological 
Survey, 7.5-minute, Topanga Quadrangle, 1952 (pho- 
torevised 1967), Santa Monica Mountains, Los Angeles 
County, southern California. Santa Susana Formation. 
Age: Late Paleocene (“Martinez Stage’). Collector: J. 
Champeny, June 1961. Same as UCLA loc. 4433. 

LACMIP 24716. Approximately 3160 ft. (1000 m) ele- 
vation, on dip slope of Redrock Mountain, about 415 
m (1400 ft.) S17 W of hill 3991, sec. 1, T6N, R17W, 
U.S. Geological Survey, 7.5-minute, Liebre Mountain 
Quadrangle, 1958 (photorevised 1974), NW San Ga- 
briel Mountains, Los Angeles County, California. San 
Francisquito Formation. Age: Late Paleocene (‘““Mar- 
tinez Stage”). Collector: E. C. Jestes, August 1963. Same 
as UCLA loc. 4716. 

LACMIP 27023. Above drop off at about 1275 ft. (400 
m) elevation, 100 m (325 ft.) NE of quarry symbol in 
Trailer Canyon, below white algal limestone, U.S. Geo- 
logical Survey, 7.5-minute, Topanga Quadrangle, 1952 
(photorevised 1967), Santa Monica Mountains, Los An- 
geles County, southern California. Santa Susana For- 
mation. Age: Late Paleocene (‘““Martinez Stage’’). Col- 
lectors. L. R. Saul and J. Alderson, June 1982. Same 
as UCLA loc. 7023. 

LACMIP 27203. West-flowing tributary to Arroyo Seco, 
approximately 160 m W of the Indians Road, approx- 
imately 3.5 km N and 0.5 km E of the SW corner of 
U.S. Geological Survey, 7.5-minute, Junipero Serra Peak 


Page 330 


Quadrangle, 1949, northern Santa Lucia Range, Mon- 
terey County, California. Unnamed mudstone. Age: 
Tentatively, late Paleocene (“Martinez Stage’). Col- 
lector: V. M. Seiders, 1982. Same as loc. 1 of SEIDERS 
& Joyce (1984:fig. 3). 

LSJU 1106. “Santa Ynez Quad.; west bank of the East 
Fork of Cachuma Creek, just north of right-angled bend 
in stream, R28W, TON, 3% miles west and *% mile south 
(to scale of U.S.G.S. topographic map) of intersection 
of Long. 119°49'W and Lat. 34°40'N”’ (KEENAN, 1932: 
79), Sierra Blanca Limestone, Santa Barbara County, 
southern California. Same as UCMP loc. A-2990 (see 
below) = UCMP loc. 4124 = CSUN loc. 955. 

UCMP A-2990. “Limestone near Cachuma Canyon.” Si- 
erra Blanca Limestone. Age: Early Ecoene. Collector: 
R. N. Nelson, early 1920s. Same as UCMP loc. 4124 
= LSJU loc. 1106 = CSUN loc. 955. 

UCMP 4124. Same as UCMP loc. A-2990, see above. 

WENTWORTH field loc. 730. “Near base of the sea cliff 
in a 3-m-thick bed of pebble conglomerate with a matrix 
of very poorly sorted clayey sandstone. The bed lies near 
the top of a section of sandstone and conglomerate which 
is overlain by mudstone and fine-grained sandstone” 
(WENTWORTH, 1966:181); 1.35 km N and 1.4 km W 
of SE corner of U.S. Geological Survey, 7.5-minute, 
Stewarts Point Quadrangle, 1978, Sonoma County, 
northern California. German Rancho formation (infor- 
mal). Age: Late? Paleocene. Collector: C. M. Went- 
worth, circa 1963. 


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ADDENDUM 


Recent collecting by William P. Elder (U.S. Geological 
Survey, Menlo Park) near Stewarts Point in northern 
California has yielded several specimens of Campanile gree- 
nellum from the Paleocene part of the German Rancho 
formation in the same area that WENTWORTH (1966, 1968) 
reported this species. Elder plans to include a discussion 
and figures of these specimens as part of a paper on the 
molluscan paleontology of the Cretaceous and Paleocene 
rocks in this area. 


The Veliger 36(4):332-342 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Larval Morphology of the Scallop 


Argopecten purpuratus as Revealed by 


Scanning Electron Microscopy 


GILDA BELLOLIO, KARIN LOHRMANN anpb ENRIQUE DUPRE 


Departamento de Biologia Marina, Facultad de Ciencias del Mar, 
Universidad Catolica del Norte, Casilla 117 Coquimbo, Chile 


Abstract. Larval development of the scallop Argopecten purpuratus (Lamarck, 1819) is described 
from trochophore stage to metamorphosis using scanning electron microscopy. The trochophore developed 
by about 12 hr post fertilization (20-22°C), the early D-stage veliger developed by about 24-36 hr post 
fertilization, and the larval stage is about 16-20 days in duration. The ready to metamorphose veliger 
larvae have a mean length of 231 wm. The larval hinge (provinculum) has a constant length during the 
larval life and no ligament is seen before metamorphosis. The development of A. purpuratus follows in 
general that described for other pectinids. Some differences in larval morphclogy from that of other 
pectinids (7.e., ornamentation of prodissoconch I and hinge morphology) are discussed. 


INTRODUCTION 


Pectinid larvae are gaining considerable attention due to 
the economic importance of scallops and the availability 
of larvae in laboratory and hatchery cultures. Although 
numerous studies have investigated various aspects of lar- 
val pectinid development (D1x & SJARDIN, 1975; Dix, 
1976; DISALVO et al., 1984; ROSE & Dix, 1984; PAULET 
et al., 1988; HODGSON & BOURNE, 1988; ROSE et al., 1988) 
few have described embryonic and larval morphology in 
detail. SASTRY (1965) characterized the morphology of lar- 
val and post-larval stages of Argopecten irradians concen- 
tricus (Say, 1822) and HopGsoN & BURKE (1988) de- 
scribed in detail the embryonic and larval morphology of 
Chlamys hastata (Sowerby, 1843). Some studies have pro- 
vided ultrastructural details of larval organs in Pecten max- 
imus (Linnaeus, 1758): the morphogenesis of the larval 
valves (LE PENNEC, 1974), the ultrastructure of the stat- 
ocysts (CRAGG & Nott, 1977), the glands of the larval 
foot (GRUFFYDD et al., 1975), the major components of the 
musculature (CRAGG, 1985), and the ciliated rim of the 
velum (CRAGG, 1989). In order to identify bivalve larvae 
within the plankton, or characterize larval developmental 
stages, hinge morphology in several pectinids has been 
described (LE PENNEG, 1974, 1980; Dix, 1976; Lurz et 
al., 1982, 1985; URIBE et al., 1982; ROSE & Dix, 1984; 
TREMBLAY et al., 1987; ROSE et al., 1988). Recently CRAGG 
& Crisp (1991) have published a comprehensive review 


of the biology of scallop larvae that includes morphology, 
physiology, behavior, distribution, and rearing method- 
ology, among others. 

The scallop Argopecten purpuratus is a functional her- 
maphrodite inhabiting the northern coast of Chile and the 
southern coast of Peru. Although it is massively produced, 
few studies have been carried out on this species and they 
have been mainly concerned with mass culture (DISALVO 
et al., 1984), population dynamics (WOLFF, 1987, 1988), 
chromosome number (VON BRAND e¢ al., 1990), and bio- 
chemical composition (MARTINEZ, 1991). The objective of 
this study is to describe the morphology of A. purpuratus 
from the trochophore stage up to metamorphosis, providing 
detailed descriptions of the trochophore, valves, velum, 
muscles, digestive system, foot, and gills. 


MATERIALS anpD METHODS 


Trochophore, veliger, and pediveliger larvae were obtained 
from the hatchery facilities at the Universidad Catolica del 
Norte, Coquimbo, Chile, where this species is cultured 
according to the method of DISALVo et al. (1984) at a 
temperature of 20-22°C. 

Specimens were relaxed using 1:1 15% solution of MgCl, 
and seawater at room temperature (16-18°C) for 1-5 min, 
and fixed in 2% glutaraldehyde in 0.025 M cacodylate- 
buffered seawater at pH 8.3 (TURNER & BOYLE, 1975). 
The specimens were dehydrated in a graded series of eth- 


G. Bellolio et al., 1993 


Page 333 
Bay 7h 
on yy i. “f ad . 9 ; 


=e i 


Explanation of Figures 1 to 5 


Figure 1. Early trochophore larva with partially removed vitelline 
envelope; prototroch (p) and primary trochoblasts (*); invagi- 
nation of the shell field (arrowhead); apical tuft (at). SEM. Scale 
bar = 10 um. 

Figure 2. Late trochophore larva with evaginating shell field 
(sf); telotroch (te); prototroch (p), vitelline envelope (ve). SEM. 
Scale bar = 10 um. 


Figure 3. Anterolateral view of trocophore; apical plate (ap) with 
apical tuft (at); cilium (cl). SEM. Scale bar = 2 um. 


Figure 4. Dorsal view of late trochophore larva with developing 
shell field (sf); hinge line (hl). SEM. Scale bar = 5 um. 

Figure 5. Early D-stage larva; valve (va); thickened border (*); 
developing velum (ve); hinge line (hl). SEM. Scale bar = 10 um. 


Page 334 The Veliger, Vol. 36, No. 4 


Explanation of Figures 6 to 12 


Figure 6. Early D-stage larva withh calcified valves; prodisso- Figure 7. External view of right valve of D-stage larva; prodisso- 
conch I (pI); velum (ve); apical tuft (at). Note punctate-stellate conch I (pI); prodissoconch II (pII); punctate region (*); stellate 
ornamentation on external surface of valve. SEM. Scale bar = region (**). SEM. Scale bar = 20 um. 


10 um. 


G. Bellolio e¢ al., 1993 


Page 335 


anol, critical point dried using CO, as a transitional fluid, 
and mounted on double scotch tape (DST). The valves of 
some larvae were removed by slightly pressing and lifting 
a wooden pick wrapped in DST. Samples were gold coated 
and examined on a JEOL JSM T300. Whole mounts 
were made by adding Orange G stain to the 95% ethanol 
solution during the dehydration process and mounting in 
Entellan Mounting Medium (Merck). 

In order to remove the vitelline envelope, some troch- 
ophore larvae were treated with 1 mM EDTA in calcium- 
free seawater for 5 min before fixation. 

Shell dimensions, measured by light microscopy, were 
length (anteroposterior distance parallel to hinge), height 
(dorsoventral distance from hinge line or umbo to ventral 
margin of shell), and provinculum length (distance be- 
tween outside denticles along the hinge line) for 30 spec- 
imens at each larval stage. 


RESULTS 
Trochophore 


The trochophore stage is attained after 8-12 hr post- 
fertilization (pf) at a temperature of 20-22°C and has a 
mean length of 70 um. The gastrula does not hatch from 
its vitelline envelope; the latter is maintained through the 
trochophore stage, being shed gradually until the formation 
of the D-stage veliger. The trochophore is typically pyr- 
iform with a well-developed 15-20-um broad prototroch 
of simple cilia that surrounds the broader part of the larva; 
these cilia develop from three to four rows of primary 
trochoblasts (Figure 1). The prototroch cilia are the first 
to develop, while the telotroch is visible only in the late 
trochophore stage; the latter is formed by a narrow band 
of simple cilia that surround the base of the larva (Figure 
2). The apical tuft is situated in the center of the apical 
plate and is formed by a group of 28-32 clustered cilia 
15-20 um long (Figure 3). The invagination of the shell 
gland occurs very early, at the gastrula stage; it is located 
on the dorsal surface of the trochophore and is visible as 
a transverse crack (Figure 2). The mouth opening is located 
opposite to the shell gland on the ventral surface and, due 
to the presence of the vitelline envelope, is hardly visible 
as a round pit. 


Veliger and Pediveliger Larvae 


Valves: The evagination of the shell gland takes place at 
a late trochophore stage, and the shell field consists of two 


—_— 
Figure 8. Provinculum of 2-day-old larva; denticles (d); striated 
cardinal region (c). SEM. Scale bar = 10 um. 


Figure 9. Provinculum of 8-day-old larva; denticles (d); striated 
cardinal region (c); longitudinal groove (g); transverse grooves 
(arrowhead). SEM. Scale bar = 10 um. 


Figure 10. Partial external view of metamorphic larva; right valve 
(rv); dissoconch (d); byssal notch (bn); prodissoconch II (pII); 


equal, oval areas of periostracum that are divided by a 
straight mark that corresponds to the hinge line (Figure 
4). The oval shell field is surrounded by a thicker border 
(Figure 5) that probably corresponds to the limit of the 
shell gland; it disappears once the valves are calcified. The 
time of calcification was not observed, but by 20 hr pf most 
larvae had calcified valves. The prodissoconch I has a 
central round area, about 20 um in diameter, with pits 
and radial striations. This configuration has been termed 
a “punctate-stellate pattern” (CARRIKER & PALMER, 1979) 
(Figure 6). By 24-36 hr pf, the prodissoconch I has grown 
and both valves are able to contact each other while en- 
closing completely the soft body of the larva. At this point 
commarginal growth lines appear in the prodissoconch, 
which is now known as prodissoconch II (Figure 7). In 
this stage the valves have three symmetrical denticles at 
each side of the hinge line and a slightly striated cardinal 
region is visible (Figure 8). The mean hinge line length 
is 69 um and the valves measure 107 wm in length and 
83.3 um in height. The provinculum or larval hinge of the 
8-day-old larva presents five symmetrical denticles on ei- 
ther side; each denticle presents a groove along its crown 
and some transverse ridges on the sides; the cardinal region 
is striated (Figure 9), and the mean hinge line length is 
95 wm. The provinculum is maintained through the rest 
of the larval life; there is no increase in its length or in 
the number of denticles, and the valves are symmetrical 
up to metamorphosis. When pediveligers reach a mean 
shell length of 231 + 10 um they are fully competent to 
metamorphose. The dissoconch or adult shell appears once 
the pediveliger has settled (16 to 20 days pf) and meta- 
morphosis is completed. The texture of the dissoconch is 
clearly different from that of the prodissoconch; both valves 
are more flexible and break easily with manipulation. The 
secretion of the adult left valve is initiated first and is 
marked by a pitted appearance and weak radial and con- 
centric striations while the right valve presents a prismatic 
ornamentation (Figures 10, 11). The byssal notch is formed 
in the latter during metamorphosis (Figures 10, 12). The 
ligament and the ligament pit were observed only in meta- 
morphic larvae. 


Digestive system: At 48 hr pf, the ““D” larva has a de- 
veloped digestive system, which is not basically different 
from the adult stage. At 8 days pf it consists of a mouth 
located under the velum at the posterior side, a foregut, a 
stomach, a digestive gland, an intestine, and an anus that 
is located dorsal to the mouth (Figure 13). The mouth is 


left valve (lv). SEM. Scale bar = 20 um. Insert: detail of prismatic 
structure of right valve. SEM. Scale bar = 5 wm. 


Figure 11. Anterior view of whole metamorphic larva; left valve 
(lv); right valve (rv); dissoconch (d). SEM. Scale bar = 25 um. 


Figure 12. Lateral view of left valve (lv) of metamorphic larva; 
byssal notch (*) viewed through the left valve; branchial filaments 
(bf). LM. Scale bar = 50 um. 


Page 336 


The Veliger, Vol. 36, No. 4 


Explanation of Figures 13 to 18 


Figure 13. Lateral view of left valve (lv) of 8-day-old veliger 
larva; foregut (fg); mouth (m); stomach (st); digestive gland (dg); 
intestine (in); anus (a); mantle cavity (mc); velar retractor muscles 
(arrows). LM. Scale bar = 25 um. 


Figure 14. Lateral view of anterior region of 8-day-old larva; 
mouth (m); postoral cilia (po); adoral cilia (ao); preoral cilia (pr); 
left valve (lv). SEM. Scale bar = 10 um. 


Figure 15. Internal view of a late veliger stage larva; mouth (m); 
foregut (fg); stomach (st); digestive gland (dg); intestine (in); 
rectum (r); anus (a). SEM. Scale bar = 20 um. 


Figure 16. Detail of digestive gland surface of an early pediveliger 
larva; stellate cell (sc); digestive gland (dg). SEM. Scale bar = 
2 um. 

Figure 17. Internal view of a late veliger stage larva; rectum (r); 
anus (a); posterior adductor muscles (pa). SEM. Scale bar = 10 
ym. 

Figure 18. Detail of Figure 17. Opening of the anus (a) with 
cilia (arrows); rectum (r). SEM. Scale bar = 2 um. 


G. Bellolio et al., 1993 


surrounded dorsally by postoral cilia and ventrally by adoral 
cilia (Figure 14). A postanal tuft of a few simple cilia is 
placed dorsal to the anus. The mantle cavity is evident at 
this stage of development. 

On the late veliger-pediveliger stage, the foregut is fun- 
nel shaped and continues into the stomach, which has a 
smooth surface (Figure 15). The digestive gland surrounds 
each side of the stomach and presents on its surface a netlike 
array of prolongations from a few stellate cells (Figure 16) 
that probably correspond to a nerve net. The intestine coils 
once and the rectum passes dorsal to the posterior adductor 
muscle (Figure 17). The opening of the anus is located in 
the mantle cavity, dorsal to the larval mouth, and cilia 
project from its lumen (Figure 18). 


Muscles: In 6-8-day-old veligers, the velar retractor mus- 
cles run obliquely in an anterior-posterior direction. They 
branch at their insertion in each valve; the same is observed 
at their insertion in the velum (Figures 13, 19, 20), and 
the branching continues as the larva grows. A maximum 
of four pairs of velar retractors was observed. 

Early veliger larvae have two anterior adductor muscles 
(Figure 20) and are the only adductors present in this 
stage. The posterior adductor muscle is formed at a late 
veliger stage (11-day-old) by a series of muscle bundles 
(Figure 21) that develop into the posterior adductor mus- 
cle. The anterior adductors are not observed after meta- 
morphosis. 


Velum: The larval velum is located at the posteroventral 
end of the larva (Figure 22). It is oval shaped, surrounded 
by cilia, and represents the locomotory and feeding organ 
of the larva. The apical tuft disappears at early prodis- 
soconch II stage. The most pronounced ciliary band cor- 
responds to the preoral band formed by long compound 
cilia (Figure 23). When deciliation is induced by excess 
of MgCl,, the preoral band is seen to be derived from two 
to three rows of cells, each bearing five to six compound 
cilia and each one formed by the clustering of about 12 
simple cilia (Figure 24). External to the preoral band there 
is an adoral band of simple cilia that are shorter than the 
preoral ones except for those on the ventral side of the 
mouth, which are longer (Figure 23). A postoral band is 
situated around the dorsal side of the mouth. Some simple 
cilia are present inner to the preoral band, but they are 
not organized as a well-defined band. During metamor- 
phosis the velum can be shed completely as one unit or 
can be deciliated gradually before being histolyzed. The 
cilia continue beating on their own for up to 10-15 min, 
and they are probably shed with their basal structures 
(Figure 25). 


Foot and gills: At 9-10 day pf a foot primordium is 
observed in the mantle cavity between the mouth and the 
anus. A ciliated heel and a nonciliated toe rudiment are 
distinguished. The byssal duct is observed in the toe-heel 
junction. At this time the gill rudiments emerge from the 


Page 337 


mantle at either side of the foot (Figures 26, 27). At 15 
days pf, the foot is well developed and the toe has length- 
ened; all the ventral surface of the toe and heel is densely 
covered with simple cilia. The lateral surface of the foot 
is nonciliated. The foot is fully functional and larvae are 
seen either crawling on the substrate or swimming. A 
ciliated duct is observed at the base of either side of the 
foot (Figures 29, 30). The gills have developed in five pairs 
of ciliated filaments located at each side in the mantle 
(Figure 12). 

The inner mantle fold shows two kinds of grouping of 
cilia: type ‘“‘a” that consists of a group of up to ten cilia of 
1.7 to 1.8 um length emerging from a protuberance, and 
type ‘““‘b” that consists of a single cilium of 1.0 to 2.1 wm 
length projecting from a circular depression. Both are al- 
ternately distributed along the mantle fold (Figures 27, 
28). 


DISCUSSION 


The development of Argopecten purpuratus follows in gen- 
eral that described for other pectinids (SAsTRY, 1965; 
HODGSON & BURKE, 1988; CRAGG & Crisp, 1991). Al- 
though several authors have reported the time of devel- 
opment of some stages of pectinid larvae (Table I), inter- 
specific comparisons become difficult because experimental 
temperatures, as well as rearing conditions, are not uni- 
form. Nevertheless, it may be noted that the trochophore 
and early D-stage larvae of A. purpuratus are attained in 
a shorter time than for A. irradians concentricus reared at 
a higher temperature (24 + 1°C), whereas metamorphosis 
is reached within the same time for both species. The mean 
lengths at metamorphosis for all species in Table 1 are 
within a similar range of 200-250 wm with the exception 
of Amusium ballot: (Bernardi, 1861), which metamorphos- 
es over a wide range of lengths, from 172 to 374 um. The 
size of metamorphic larvae of A. purpuratus is well within 
the range described for other pectinids (CRAGG & CRISP, 
1). 

The maintainance of the vitelline envelope in the troch- 
ophore stage and its gradual shedding during larval de- 
velopment have not been reported before. In a similar study 
of Chlamys hastata (HODGSON & BURKE, 1988) the vitelline 
envelope was shed in the gastrula stage, when the larva 
hatches; other studies of pectinids do not refer to this pro- 
cess. 

The punctate-stellate pattern on the prodisoconch I of 
Argopecten purpuratus is similar to that described for other 
pectinids (LUCAS & LE PENNEC, 1976; HODGSON & BURKE, 
1988) and for other bivalve larvae (ANSELL, 1961, 1962; 
CARRIKER & PALMER, 1979; WALLER, 1981). However, 
in A. purpuratus the pattern is circular and covers an area 
of about 20 wm in diameter, about half the size of the 
region of Chlamys hastata that is oval shaped. The pattern 
in A. purpuratus also differs from that described for other 
species (CARRIKER & PALMER, 1979; WALLER, 1981), sug- 


Page 338 


The Veliger, Vol. 36, No. 4 


Explanation of Figures 19 to 24 


Figure 19. Internal view of 8-day-old veliger larva; branched 
velar retractor muscles (vr); insertion on internal surface of valve 
(i). SEM. Scale bar = 10 pum. 


Figure 20. Internal view of 8-day-old veliger larva; anterior 
adductor muscles (aa). Velar retractor muscles (vr). SEM. Scale 
bar = 10 um. 


Figure 21. Internal view of 11-day-old veliger larva showing 
developing posterior adductor muscle (pa); insertion on internal 
surface of valves (i). SEM. Scale bar = 10 wm. 


Figure 22. External view of transition trochophore to D-stage 
larva, about 18 hr pf; left valve (lv); velum (ve); postanal tuft 
(pat); anus (a). SEM. Scale bar = 10 um. 


Figure 23. Mouth region of 8-day-old veliger larva; preoral band 
(pr); adoral band (ao); postoral band (po); mouth (m). SEM. 
Scale bar = 10 um. 


Figure 24. Detail of deciliated preoral band cells (poc) of 12- 
day-old veliger larva, showing cilia “scars” rows (arrows). SEM. 
Scale bar = 5 um. 


G. Bellolio e¢ al., 1993 


Explanation of Figures 25 to 30 


Figure 25. Cilia (ci) shed from velum during settlement; basal 
structure (*). SEM. Scale bar = 5 um. 


Figure 26. Internal view of mantle cavity of early pediveliger 
larva; foot primordium (fp); heel (h); toe rudiment (t); gill ru- 
diments (gr). SEM. Scale bar = 10 um. 


Figure 27. Internal view of mantle cavity of 10-day-old veliger 
larva; gill rudiment (gr); mantle fold (mf). SEM. Scale bar = 5 
um. 


Figure 28. Detail of Figure 27; mantle fold (mf); ciliary grouping 
type ‘“‘a” (a); ciliary grouping type “b” (b). SEM. Scale bar = 
2 um. 

Figure 29. Mantle cavity of 15-day-old pediveliger larva; foot 
(ft); toe (t); heel (h); ciliated ventral surface (*); ciliated duct 
(cd). SEM. Scale bar = 20 um. 


Figure 30. Detail of Figure 29; ciliated duct (cd). SEM. Scale 
bar = 10 um. 


Page 340 


The Veliger, Vol. 36, No. 4 


Table 1 


Time of development of some stages of pectinid larvae under laboratory conditions. pf = post-fertilization. 


Trochophore 
Mean 
Temp Hours length 
°C pf (um) 
Argopecten purpuratus 
(present study) 20-22 8-12 70 
Chlamys hastata 
(Hopcson & BURKE, 
1988) 14-16 30 60 
Argopecten irradians 
concentricus 
(SasTRY, 1965) 23-25 24 — 
Chlamys (Chlamys) 
asperrimus 
(ROsE et al., 1984) 17-18 24 70 


Pecten maximus 
(GRUFFYDD, 1972) 16 20 — 


Amusium balloti 
(ROSE et al., 1988) 


gesting this character might be of taxonomic importance 
and a possible tool for identification of early planktonic 
stages. 

The prodissoconch II ornamentation (commarginally 
striate) does not differ from that of other pectinids 
(MERRILL, 1961; LUTZ et al., 1982; URIBE et al., 1982; 
HopGson & BURKE, 1988; CRAGG, 1989) and the initi- 
ation of it occurs about the same time, when the prodis- 
soconch I is able to enclose the soft body of the larva. This 
supports the suggestion of WALLER (1981) that the prodis- 
soconch II is secreted by the rim of the mantle and the 
prodissoconch I is secreted by the shell gland. 

The basic hinge morphology of Argopecten purpuratus 
is similar to that of other pectinids—hinge teeth at each 
end with a thin, slightly striated cardinal ridge that lacks 
teeth. Nevertheless, there is variability in the total number 
of teeth as well as the number on the anterior and posterior 
hinge side. They vary from a total of seven teeth for Chlam- 
ys asperrima (Lamarck, 1819) (RosE & Dix, 1974) with 
three and four hinge teeth at each end, to 10 or 12 sym- 
metrically placed on C. hastata (HODGSON & BURKE, 1988) 
(Table 1). In A. purpuratus the number of teeth increases 
during larval development, although the provinculum length 
remains constant throughout larval life, indicating that 
teeth are added to the inside; this was described for the 
first time in Chlamys hastata (HODGSON & BURKE, 1988). 
Also, as described for the latter species, A. purpuratus pre- 
sents on each denticle a longitudinal groove and transverse 
ridges on the sides. 

The dissoconch of Argopecten purpuratus is similar in 
shape and ornamentation to Placopecten magellanicus 
(Gmelin, 1791) (MERRILL, 1961) and to Chlamys hastata 


18-19 28 85.5 


Early D Metamorphosis 
Mean Mean 
Hours length Days length 
pf (um) pf (um) 
24-36 107 16-20 2315 =O 
50 105 40 240 
48 101 15-19 190-200 
48 108 20 170-250 
40-50 — 33-38 250 
48 123 22-27 172-374 


(HODGSON & BURKE, 1988) and to the general description 
of other pectinid dissoconchs (CRAGG & Crisp, 1991). In 
A. purpuratus the ligament pit seems to be characteristic 
of metamorphic larvae, so it is possible that the ligament 
appears in larvae that are in the process of metamorphosis. 
A ligament pit was not observed in ready to metamorphose 
larvae as described for Chlamys hastata (HODGSON & BURKE, 
1988). 

The arrangement and number of velar retractors and 
the branching of the retractors that increases as the larva 
grows is similar to Pecten maximus (CRAGG, 1985). Also, 
the anterior adductor muscle that is formed by two columns 
and the posterior adductor that is formed by several muscle 
bundles not organized in columns corresponds to those 
described for P. maximus. We did not do further histolog- 
ical analysis to determine which part of each adductor 
corresponds to striate or to smooth muscle, as this was not 
possible to do by means of SEM. 

In Argopecten irradians concentricus (SASTRY, 1965) the 
sensory tentacles appear on post-larvae as small papillary 
projections on the mantle margin; the eyes appear later as 
pink protuberances on the mantle alternating with the 
tenctacles. In A. purpuratus the protuberances with clusters 
of cilia may be interpreted as developing tentacles. The 
ciliary duct observed on the foot probably conforms to the 
statocyst duct as in Pecten maximus (CRAGG & NOTT, 
1977) and in Ostrea edulis (WALLER, 1981). 


ACKNOWLEDGMENTS 


Weare grateful to the Production Unit of the Aquaculture 
Department of Universidad Catolica del Norte for pro- 


G. Bellolio et al., 1993 


viding the scallop larvae. This research was supported by 
a grant from the Direccion General de Investigacion, Ex- 
tension y Asistencia Técnica of Universidad Catolica del 
Norte. 


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The Veliger 36(4):343-350 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


A Review of Pitar (Hyphantosoma) Dall, 1902 
(Veneridae: Pitarinae) and a Description of 


TC i MesLoul SP. OV. 


MARY ELLEN HARTE 


1180 Cragmont Ave., Berkeley, California 94708, USA 


Abstract. 


Hyphantosoma Dall, 1902, a tropical subgenus of Pitar (Bivalvia: Veneridae), is charac- 


terized by fine zigzag sculpture. It includes six fossil species: four from the Caribbean, one from the 
eastern Pacific, and one from New Zealand. Of the five living species, three occur in the eastern Pacific. 
A fourth species, P. (H.) intricata (Dautzenberg, 1907), occurs in the west Pacific. A fifth species, P. 
(H.) festowi sp. nov., is herein described from Tahiti, French Polynesia. 


INTRODUCTION 


Unlike other major subfamilies in the Veneridae Rafin- 
esque, 1815, no recent published revision exists of the 
Pitarinae Stewart, 1930, and it remains one of the least 
understood venerid subfamilies. The nominate genus Pitar 
Romer, 1857, contains 50 or more extant species; KEEN 
(1969) lists 11 extant subgenera, including Hyphantosoma 
Dall, 1902. Hyphantosoma includes pitarine clams with 
fine zigzag sculpture on their valves, a rare sculptural 
pattern within the family. Here I review the species of 
this taxon, describe their past and present distribution, 
discuss their relationships with other pitarine taxa, and 
describe a new species. 


Museum abbreviations: Academy of Natural Sciences at 
Philadelphia, ANSP; National Science Museum at Tokyo, 
NSMT; United States National Museum, USNM; Uni- 
versity of California Museum of Paleontology, UCMP. 


SYSTEMATIC ACCOUNT 
Genus Pitar Romer, 1857 


Subgenus Hyphantosoma Dall, 1902 


Hyphantosoma DALL, 1902:354; type species (original des- 
ignation): Cytherea (Circe) carbasea Guppy, 1866. 


Definition: Valves have fine, chiseled zigzag sculpture on 
part or all of the surface; ovate to subovate and subtrigonal 
profiles; large lunules; well-developed anterior lateral teeth; 
smooth internal margins. 


Description: DALL (1902) described the taxon simply as 


“shell with zigzag sculpture on the surface like Textzvenus 
Cossmann, of the Venerine series,” and the sculpture itself 
as “‘fine zigzag chiseling of the surface.” Zigzag sculpture 
is often restricted to the sides; it is evident over the entire 
surface of Hyphantosoma aletes Hertlein & Strong, 1948, 
but small specimens lack the sculpture, and it is easily 
eroded off larger specimens (HERTLEIN & STRONG, 1948). 
Zigzag sculpture is more sharply defined in the tropical 
mid-and western Pacific species. 

Extant species of Hyphantosoma have ovate valves, typ- 
ically with slightly to more pronounced subquadrate pos- 
terior ends. The escutcheon is often well defined by a slight 
ridge, an uncommon state within Pitarinae. The lunule is 
large, moderately obese, and distinctly, if shallowly, in- 
cised. The cardinal teeth are typical of Pitarinae: the right 
anterior and posterior teeth are dorsally attached, as are 
the left anterior and median teeth, and the right anterior 
tooth is partially detached from the hinge plate. The left 
anterior lateral tooth is well developed, compact, and either 
close to or moderately separate from the cardinal teeth. 
The sculpture is of fine, polished, indistinct growth bands, 
superimposed partly or entirely by fine, nested, zigzag 
threads. The pallial sinus is well developed, moderately 
deep, and triangular, with a rounded apex. The valves are 
white, porcelaneous, often patterned with brown marks or 
rays, and range from 2 to 8 cm in length. 


Remarks: DALL (1902) observed that among American 
taxa the surface zigzag sculpture is present in Oligocene 
species, becoming obsolete in the Pliocene and is present 
only within the shell matrix for Recent species, becoming 
evident in worn specimens, with color patterns that fre- 


Page 344 


The Veliger, Vol. 36, No. 4 


quently follow the zigzag pattern. In fact, zigzag sculpture, 
although not sharply highlighted, occurs on the surface of 
all three Recent American species. Traces of zigzag sculp- 
ture occur on the posterior surface of the type of Hyphan- 
tosoma pollicaris (Carpenter, 1864) (USNM 1372), and of 
H. hertleini Olsson, 1961 (OLSSON, 1961; herein, Figure 
2c). 


Distribution: The taxon is recorded in fossils ranging from 
the Early Oligocene to early Pleistocene in the Caribbean 
(WooDRING, 1982). Several fossil species are recorded from 
this area and one species from New Zealand. The bio- 
geographic range of living species is exclusively subtropical 
and tropical Pacific. In the west Pacific, specimens of Hy- 
phantosoma have been recorded from the Philippines (HABE 
& OKUTANI, 1983), southern Japan (HABE, 1981; 
MATSUKUMA, 1984), Truk and Ponape of the Eastern 
Caroline Islands (MATSUKUMA, 1984), and Tahiti in the 
south Pacific (HARTE, 1992). I have personally collected 
beachdrift specimens from Java, Indonesia, near Jakarta. 
In the eastern Pacific, Hyphantosoma occurs from the Gulf 
of California to Peru (KEEN, 1971). All species are un- 
common to rare, and occur in subtidal offshore sediments 
of mud, gravelly or shelly sand (HERTLEIN & STRONG, 
1948), or coralline sand (HARTE, 1992). 


Fossil Species 
Pitar (Hyphantosoma) carbasea (Guppy, 1866) 
(Figure la—d) 


Cytherea (Circe) carbasea GUPPY, 1866:292, pl. 18, fig. 13; 
PALMER, 1927:56, pl. 10, figs. 1, 4, 13, 14. 


Description: Length, 36 mm; height, 30 mm; semidiam- 
eter, 15 mm. A thin, ovate shell sculptured with close, fine, 
distinct radial grooves that curve upward laterally and 
broadly zigzag medially (WOODRING, 1925). 


Remarks: Guppy (1866) noted that the sculpture is similar 
to that of Gafrarium divaricatum (Gmelin, 1791), although 
the latter’s sculpture consists of the threads describing a 
few large zigzags, and not the many small zigzags char- 
acteristic of Hyphantosoma. 


Type material: Holotype, British Museum, Natural His- 
tory 64086. 


Distribution: Miocene. Bowden, Jamaica; Santo Domin- 
go. 


Pitar (Hyphantosoma) semipunctata (Conrad, 1848) 
(Figure le, f) 


Cytherea semipunctata CONRAD, 1848:134, pl. 13, fig. 19; 
PALMER, 1927:55, pl. 10, figs. 5, 9. 


Description: Length, 14 mm; height, 12 mm; semidiam- 
eter, 4 mm. An ovate shell sculptured with close, narrow 
but distinct commarginal ribs, crossed by a zigzag series 
of punctations. 


Remarks: CONRAD (1848) presents no written description 
of the species, and both his figure and those of PALMER 
(1927) do not show the zigzag series of punctations, in- 
dicating that this sculpture is weak and is dominated by 
the commarginal ribs. 


Type material: Holotype, ANSP 30658. 


Distribution: Oligocene. Vicksburg, Mississippi (type lo- 
cation). 


Pitar (Hyphantosoma) floridana Dall, 1903 
(Figure 1g) 


DALL, 1903:1267, pl. 54, fig. 10; PALMER, 1927:56, pl. 10, 
fig. 6. 


Description: Length, 29 mm; height, 24 mm; width, 17 
mm. A solid, subtrigonal shell sculptured with fine com- 
marginal threads, crossed by close, fine, faint zigzag sculp- 
ture that appears obsolete anteriorly but present elsewhere. 
Posterior end emphasized by one or two slight radial ridges; 
lunule long, rather narrow. 


Type material: Holotype, USNM 114753. 


Distribution: Lower Miocene. Chipola horizon at Alum, 
and on the Chipola River at McDonald’s farm, Florida. 


Pitar (Hyphantosoma) opisthogrammata Dall, 1903 
(Figure 11) 


DALL, 1903:1267, pl. 54, fig. 8; PALMER, 1927:58, pl. 10, 
fig. 2. 


Description: Length, 39 mm; height, 32 mm; width, 22 
mm. A subovate, somewhat trigonal shell with a slightly 
subquadrate posterior end sculptured with fine commar- 
ginal lines; fine zigzag sculpture is mostly obsolete, usually 
discernible only ventrally. Lunule deeply impressed, sharply 
incised, with a second, fainter, lunular furrow paralleling 
the ventral boundary. 


Remarks: Similar in shape to Pitar floridana, P. opistho- 
grammata has much less zigzag sculpture, no posterior 
ridge, and a distinctly different lunule. 


Type material: Holotype, USNM 109232. 


Distribution: Pliocene. Marl of Shell Creek and Alligator 
Creek near Charlotte Harbor, Florida. 
A single fossil species is recorded from Panama: 


Pitar (Hyphantosoma) centangulata 
Brown & Pilsbry, 1911 
(Figure 1h-k) 


BROWN & PIxsBry, 1911:369; PALMER, 1927:264-265, pl. 
10, figs. 7, 8, 10, 12; WoOODRING, 1982:686-687, pl. 122, 
figs. 4-8, 11. 


Description: Length, 51 mm; height, 40 mm; semidiam- 
eter, 16 mm. A thin ovate shell without any posterior ridge; 


M. E. Harte, 1993 


Page 345 


Figure 1 


a-d. Pitar (Hyphantosoma) carbasea (Guppy). a. Length (L) = 36 mm. b. Hinge of right valve. c. L = 37 mm. d. 
L = 44 mm. e, f. P. (Hyphantosoma) semipunctata (Conrad). e. L = 11.5 mm. f. L = 14 mm. g. P. (Hyphantosoma) 
floridana Dall, L = 30 mm. h-k. P. (Hyphantosoma) centangulata Brown & Pilsbry. h, i. L = 52 mm. j. L = 36 
mm, semidiameter = 13 mm. 1. P. (Hyphantosoma) opisthogrammata Dall, L = 32 mm (1a-] from PALMER, 1927). 
m. P. (Hyphantosoma) sculpturata (Marshall), L = 30 mm (from BEU & MAXWELL, 1990). 


fine zigzag sculpture is obsolete dorsally but otherwise 
present. 


Remarks: The sculpture of Pitar centangulata is similar 
to that of P. floridana, although the former is larger, dif- 
ferently shaped, and lacks a posterior ridge. Observing no 
real differences in shape and areas with zigzag sculpture 
between P. centangulatus and P. carbasea, WOODRING (1982) 
distinguished them solely on the zigzag sculpture which, 
PALMER (1927) observed, was much finer in P. centan- 
gulatus. 


Type material: Holotype, ANSP 1764. 


Distribution: Early-Mid Miocene. Gatun Locks exca- 
vations of Canal Zone, Panama: Quarry on west side of 
Gatun locks. 


Marwick (1927) noted one fossil species from New 
Zealand: 


Pitar (Hyphantosoma) sculpturata (Marshall, 1918) 
(Figure 1m) 


Macrocallista sculpturata MARSHALL, 1918:272, pl. 20, figs. 
6-6a; MARWICK, 1927:594-595, pl. 41. figs. 74-76. 


Description: Length, 30 mm; height, 20 mm; width, 25 
mm. A broadly ovate to subovate shell sculptured with fine 
commarginal lines superimposed by faint fine zigzag sculp- 
ture, strongest at both ends; it is very thin (A. Beu, personal 
communication). The left anterior lateral is long, well 
separated from the cardinals, and the lunule is large. 


Remarks: BEU & MAXWELL (1990) note that the Clifden 


Page 346 


specimens differ from the Pakaurangian topotypes in hay- 
ing narrower but higher umbones and might not be con- 
specific with them. 


Type material: Holotype, TM 4567, Institute of Geolog- 
ical and Nuclear Sciences, Lower Hutt, New Zealand. 


Distribution: Upper Oligocene: Otaian-Altonian. New 
Zealand: Pakau-rangi Point, Kaipara (type location); bed 
6A, Clifden, Southland; east of the Puketoi Range, south- 
ern Hawke’s Bay. 


Key to Fossil Species of Hyphantosoma 


ll; SPACiiCks PE CIES \ = atese erase meee uals enone ment wd 2 
ISSA tam th C8 Pe Cl CS yess a eee een Se oe 3 
2. New Zealand species; ovate; sculpture of many fine 

ZAEZ ATS eBid sack Pa led RS he eee er A sculpturata 
2 


Eastern Pacific species; ovate; zigzag sculpture of 
curving radials laterally and broad zigzag me- 
Ural yy ssi Saas ean Sens ad centangulata 

3. Zigzag sculpture consists of series of punctations 

crisscrossing distinct commarginal cords 
SN ae ore Oo Ne SE semipunctata 
3. Zigzag sculpture consists of fine, close-set threads 


ANG STOOVES wes emenen eel etn nae) aaeee at me tens ven Sieur 4 
4. Shell ovate, thin; zigzag sculpture of curving radials 

laterally, broad zigzag centrally ww. carbasea 
4. Shell subovate to subtrigonal; zigzag sculpture of 

SEVET AE ZS Za Ose eee ee ieee eee eee ie ee 5 


5. Subtrigonal; posterior end with 1 or 2 slight radial 
ridges; zigzag sculpture absent anteriorly . floridana 

5. Subovate, somewhat subtrigonal; posterior end 
slightly subquadrate, with no radial ridges; zig- 
zag sculpture usually only discernible ventrally 
aE Le Mee Os Dose oe ee opisthogrammata 


Living Species 


Of the five living species, three occur in the eastern 
Pacific: 


Pitar (Hyphantosoma) aletes Hertlein & Strong, 1948 
(Figure 3F) 


HERTLEIN & STRONG, 1948:172-173, pl. 1, figs. 9, 11-13; 
OLSSON, 1961:277-278, pl. 49, fig. 3; KEEN, 1971:170, 
fig. 404. 


Description: Length, 54 mm; height, 46 mm; width, 34 
mm. A white, subovate, somewhat subtrigonal shell sculp- 
tured with fine, polished commarginal lines, superimposed 
by fine close zigzag sculpture covering most of the shell. 
Zigzag sculpture is absent on juveniles and possibly some 
specimens (HERTLEIN & STRONG, 1948). The pallial sinus 
is less than half the shell length. 


Remarks: HERTLEIN & STRONG (1948) noted that Pitar 
aletes closely resembles P. carbasea but has a more angular 


The Veliger, Vol. 36, No. 4 


posterior end. OLSSON (1961) stated that it closely resem- 
bles P. pollicaris (Carpenter, 1864), below, but P. aletes is 
deeper (height vs. length), more trigonal and more convex. 


Type material: Holotype, California Academy of Sci- 
ences, CAS 065554. 


Distribution: Gulf of California to Costa Rica. Depth 77- 
110 m. Rare. 


Pitar (Hyphantosoma) hertleini Olsson, 1961 
(Figure 2c, d) 


OLSSON, 1961:276-277, pl. 45, figs. 6-6a; KEEN, 1971:170, 
fig. 405. 


Description: Length, 36 mm; height, 29 mm; width, 19.5 
mm. An ovate shell sculptured with fine polished com- 
marginal lines, with traces of zigzag sculpture evident on 
its posterior end, but otherwise obscure or absent. It is 
richly patterned with brown zigzag markings and radial 
rays against a cream white background. 


Remarks: OLSSON (1961) notes it is thinner, smaller, more 
strongly colored and with more convex valves than Pitar 
pollicaris, below. The patterns and coloring resemble some 
P. (Pitar) newcombianus (Gabb, 1865) from Baja Califor- 
nia, Mexico, and California, but P. hertleini has a broader 
posterior end, blunter anterior end and zigzag sculpture. 


Type material: Holotype, ANSP 218921. 


Distribution: Panama to Peru. Rare. 


Pitar (Hyphantosoma) pollicaris (Carpenter, 1864) 
(Figure 2a) 


Callista pollicaris CARPENTER, 1864:312; OLSSON, 1961:277, 
pl. 49, figs. 7-7a; KEEN, 1971:170, fig. 406. 


Description: Length, 66 mm; height, 57 mm; width, 36 
mm. A large, ovate, white shell, with zigzag sculpture 
present in adults as faint traces at the ends. Juveniles have 
zigzag markings and sculpture; pallial sinus long, extend- 
ing to nearly half the shell length (KEEN, 1971). It is the 
largest species of Hyphantosoma (Figure 1a), a large spec- 
imen measuring: length, 80 mm, height, 60 mm, width, 
39 mm (HERTLEIN & STRONG, 1948). 


Remarks: HERTLEIN & STRONG (1948) note that the spe- 
cies resembles Pitar (Pitar) prora (Conrad, 1837) (see Fig- 
ure 2b). 


Type material: Holotype, USNM 13721. 


Distribution: Gulf of California to Colombia. The species 
probably occurs just beyond the low tide line (KEEN, 1971); 
it has been dredged from sandy bottoms at 13-14 m. Rare. 

Two more species exist in the tropical west and South 
Pacific, respectively: 


M. E. Harte, 1993 


Pitar (Hyphantosoma) intricata (Dautzenberg, 1907) 
(Figure 3D, E) 


Meretric (Pitar) intricata DAUTZENBERG, 1907:333-334, pl. 
6, fig. 1. Callogonia philippinensis HABE & OKUTANI, 
1983:1-3; figs. 1-4. Pitar (Hyphantosoma) limatulum 
(Sowerby, 1851), of HABE, 1977, and MATSUKUMaA, 1984, 
non Sowerby, 1851. 


Description: Length, 50 mm; height, 41 mm; width, 31 
mm. This ovate shell is sculptured with fine, polished, 
indistinct, commarginal lines, superimposed by fine zigzag 
sculpture over most of the shell (Figure 3D, E). The um- 
bones are prominent, and the posterior end is broad and 
rounded. The left anterior lateral tooth is compact and 
relatively close to the anterior cardinal, unlike in other 
living species. The shell is often patterned with flecked or 
solid brown rays of variable width, sometimes traversed 
by concentric bands of brown. 


Type material: Holotype, Laboratoire de Biologie des 
Invertebres Marins et Malacologie collection, Museum 
National d’Histoire Naturelle, Paris. Hypotypes, NSMT 
Mo-61187, NSMT Mo-54072. 


Distribution: Kii Peninsula, Japan; the Philippines; Cel- 
ebes; Java, Indonesia; Ponape and Truk, Eastern Caroline 
Islands. Depth: 10-42 m. Uncommon. 


Pitar (Hyphantosoma) festoui Harte, sp. nov. 
(Figure 3A-C) 


Pitar (Hyphantosoma) sp.: HARTE, 1992:7, cover figs. 9-10. 


Description: Length, 22 mm; height, 18 mm; width, 14 
mm. An ovate shell sculptured with fine, polished, indis- 
tinct, commarginal lines, superimposed by fine zigzag 
sculpture over most of the shell (Figure 3A-C). It is marked 
irregularly with light brown patches of variable size, some- 
times almost forming large, irregular, compounded chev- 
rons. A bib of deep rosy red extends laterally on either 
side from the base of the umbo, skirting the border of the 
lunule, and fading anteriorly to the main part of the es- 
cutcheon. A gray concentric band, occurring medially, in- 
terrupts the otherwise white background of the type spec- 
imen. The escutcheon is fairly well defined, and marked 
with a few brown zigzags. The lunule is large, moderately 
obese, and distinctly incised. In the left valve, a compact, 
well-developed, anterior lateral tooth is moderately sepa- 
rated from the cardinal teeth. A moderately thick, trian- 
gular anterior cardinal is connected dorsally to a longer, 
wedge-shaped median cardinal. The posterior cardinal is 
a long, narrow ridge. In the right valve, there are two 
smaller anterior lateral teeth, and a short triangular an- 
terior cardinal connected to and aligned perpendicularly 
to a long, narrow, slightly bifid posterior cardinal. The 
right median cardinal is short, triangular, close to and in 


Page 347 


Figure 2 


a. Pitar (Hyphantosoma) pollicaris (Carpenter), Baja California, 
Mexico, Length (L) = 64 mm. b. Pitar (Pitar) prora (Conrad), 
Tahiti, L = 34 mm. c, d. Pitar fulminatus (Menke), Florida, L 
= 50 mm (left), P. (Hyphantosoma) hertleini Olsson, Baha Cal- 
ifornia, Mexico, L = 46 mm (right). c. Exteriors. d. Interiors. 
UCMP specimens. 


parallel with the anterior cardinal. The pallial sinus is 
deep, triangular, and rounded at the apex. 


Remarks: While the sculpture of Pitar festoui is similar 
to that of P. intricata, the anterior end of P. festoui is more 


Page 348 


The Veliger, Vol. 36, No. 4 


Figure 3 


a-c. Pitar (Hyphantosoma) festoui sp. nov., Tahiti, Holotype, L = 22 mm. a. Both valves. b. Inset of right valve, 
showing fine zigzag sculpture. c. Hinge and interior of holotype valves. d, e. Pitar (H.) intricata (Dautzenberg), 


Indonesia. d. Worn valves, L = 53 mm, 38 mm. e. Inset of larger valve, showing fine zigzag sculpture. UCMP 
specimens. f. Pitar (H.) aletes Hertlein & Strong, holotype, CAS 065554. 


M. E. Harte, 1993 


pronounced and the posterior end is narrower, and more 
subquadrate. The left anterior lateral of P. intricata is 
closer to the cardinal teeth than that of P. festowz. 


Type material: Holotype, UCMP 398606. 


Type location: Off Afaahiti, Tahiti, French Polynesia 
(149°15'N, 17°45’W). Two specimens, one of which was 
subsequently misplaced, were found in coralline sand near 
clumps of living corals at 60 m, near the end of the water 
column blue zone. 


Key to Recent Species of Hyphantosoma 


leeShelleiromatheeastern| Pacific 2 2 
1. Shell from the western or central tropical Pacific 
Na Tee NA Ae eee ats 3 
2. External color patterns absent; if present, pallial 
Simuspneariy half thejishell length. = 4 
2. External color patterns obvious; pallial sinus less 
than half the shell length 200 hertleint 
3. Umbo rose colored; left anterior lateral well sep- 
anatedetromycanginal See festou 
3. Umbo not rose colored; left anterior lateral situated 
closeito) the cardinal = intricata 
4. Pallial sinus less than half the shell length; shell 
ROUNGveSUDtGISOnale se ee aletes 
4. Pallial sinus nearly half the shell length; shell ovate 
scenic ee A ee pollicaris 
DISCUSSION 


Conchological characteristics link living Hyphantosoma 
closely to American and Pacific species of Pitar s. s. The 
pan-Pacific Pitar (Pitar) prora (Conrad, 1837), for ex- 
ample, has the somewhat well-defined escutcheon and deep, 
triangular pallial sinus characteristic of Hyphantosoma 
(Figures 2b, 3c, d). Pitar (H.) hertleini has color patterns 
similar to the eastern Pacific P. (P.) newcombianus (Gabb, 
1865), and the Caribbean P. (P.) simpsoni (Dall, 1889), 
and P. (P.) fulminatus (Menke, 1828). Pitar hertleini and 
P. fulminatus have similar hinge plates and pallial sinuses 
(Figures 2c, d). DALL (1903) linked P. sempsoni, marked 
with zigzags, to Hyphantosoma via sculpture, observing 
that erosion of specimens of P. simpsoni revealed zigzag 
sculpture; how much this might be due to selective erosion 
of either pigmented or nonpigmented parts of the shell, 
however, is unknown. 

The lunule of Hyphantosoma is similar to that of Pitar 
(Pitarenus) Rehder & Abbott and Pitar (Pitarella) Palmer, 
but the latter two taxa are generally chalky, more obese, 
and with a well-developed but narrow left anterior lateral 
tooth. While the restriction of zigzag sculpture within Pi- 
tarinae to Hyphantosoma indicates monophyly, the geo- 
graphic range of the subgenus and its similarities to both 
Pacific and Caribbean taxa of Pitar allow the possibility 
of parallel acquisition of zigzag sculpture among those 
taxa. Anatomical and biomolecular studies could further 


Page 349 


clarify the taxonomic relationship of Hyphantosoma to the 
various subgenera of Pitar. 


ACKNOWLEDGMENTS 


I thank Patrick Festou for donating holotypic material to 
the University of California (Berkeley) Museum of Pa- 
leontology, and Dr. Eugene Coan and an anonymous re- 
viewer for their constructive comments. The Paleontolog- 
ical Research Institution, and Drs. Alan Beu and P. A. 
Maxwell, of the Institute of Geological and Nuclear Sci- 
ences, Limited, kindly permitted me to reprint illustrations 
of fossil species. 


LITERATURE CITED 


Beu, A. G. & P. A. MAXWELL. 1990. Cenozoic Mollusca of 
New Zealand. New Zealand Geological Survey Paleonto- 
logical Bulletin 58:518 pp. 

Brown, A. P. & H. A. Pi“spry. 1911. Fauna of the Gatun 
formation, Isthmus of Panama. Proceedings of the Academy 
of Natural Sciences at Philadelphia 63:361-373. 

CARPENTER, P. P. 1864. Diagnoses of new forms of mollusks 
collected at Cape St. Lucas by Mr. J. Xantus. Annals and 
Magazine of Natural History, Series 3, 13:311-315. 

CONRAD, T. A. 1848. Observations on the Eocene formation, 
and descriptions of one hundred and five new fossils of that 
period, from the vicinity of Vicksburg, Mississippi; with an 
appendix. Journal of the Academy of Natural Sciences of 
Philadelphia, 2nd series, 1:111-134. 

DALL, W. H. 1902. Synopsis of the family Veneridae and of 
the North American Recent species. Proceedings of the U.S. 
National Museum 26:335-411. 

DALL, W. H. 1903. Veneracea, in Contributions to the Tertiary 
fauna of Florida. Part VI. Transactions of the Wagner Free 
Institute of Science 3:1219-1333. 

DAUTZENBERG, P. 1907. Description de coquilles nouvelles de 
diverses provenances et de quelques cas teratologiques. Jour- 
nal de Conchyliologie 55:327-341. 

Guppy, R. J. L. 1866. On the Tertiary Mollusca of Jamaica. 
Quarterly Journal of the Geological Society of London 22: 
281-295. 

HaseE, T. 1977. New and little known bivalves of Japan. Venus 
36:1-13. 

HaskE, T. (ed.). 1981. A catalogue of the molluscs of Wakayama 
Prefecture, the Province of Kii. Publications of the Seto 
Marine Biological Laboratory Special Publication Series, 
7:301 pp., 13 pl. 

Hase, T. & T. OKUTANI. 1983. A new vesicomyid bivalve and 
two new gastropods of the genera Guildfordia and Xenophora 
from the Philippines. Venus 42:1-7. 

Harte, M. E. 1992. The Veneridae of Polynesia. Xenophora 
59:4-10. 

HERTLEIN, L. G. & A. M. STRONG. 1948. Mollusks from the 
west coast of Mexico and Central America. Part VI. Zoolog- 
ica 33:163-197. 

KEEN, A.M. 1969. Veneridae. Pp. N671-688. In: R. C. Moore 
(ed.), Treatise of Invertebrate Paleontology. Geological So- 
ciety of America and University of Kansas: Lawrence. 

Keen, A. M. 1971. Sea Shells of Tropical West America. 
Stanford University Press: Stanford. 1064 pp., 22 pls. 

MARSHALL, P. 1918. Tertiary molluscan fauna of Pakaurangi 


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Point. Transactions and Proceedings of the New Zealand 
Institute 50:263-278. 

Marwick, J. 1927. The Veneridae of New Zealand. Trans- 
actions and Proceedings of the New Zealand Institute 57: 
567-635. 

MATSUKUMA, A. 1984. Intertidal bivalved molluscs collected 
from the Eastern Caroline and Marshall Islands, Western 
Pacific. Proceedings of the Japanese Society of Systematic 
Zoology No. 27:1-34. 

Oxsson, A. A. 1961. Mollusks of the tropical eastern Pacific, 
particularly from the southern half of the Panamic-Pacific 
faunal province (Panama to Peru). Panamic-Pacific Pelecy- 
pods. Paleontological Research Institution: Ithaca. 574 pp., 
86 pls. 


The Veliger, Vol. 36, No. 4 


PALMER, K. V. W. 1927. The Veneridae of eastern America, 
Cenozoic and Recent. Paleontographic Americana 1:209- 
522. 

SOWERBY, G. B. 1851. Monograph of the genus Cytherea. In: 
Thesaurus Conchyliorum 2:611-648. 

SowErRBY, G. B. 1851. Monograph of the genus Circe. In: The- 
saurus Conchyliorum 2:648-654. 

WooprInGc, W. P. 1925. Miocene mollusks from Bowden, 
Jamaica. Carnegie Institution of Washington, Publ. No. 366. 

WooprIncG, W. P. 1982. Geology and Paleontology of Canal 
Zone and adjoining parts of Panama. Description of Tertiary 
Mollusks. Pelecypods: Propeamussidae to Cuspidariidae. 
Geological Survey Professional Paper 306-F:759 pp., 42 pls. 


The Veliger 36(4):351-388 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Additions to Pacific Slope ‘Turonian Gastropoda 


by 


L. R. SAUL 


Natural History Museum of Los Angeles County, Invertebrate Paleontology Section, 
900 Exposition Boulevard, Los Angeles, California 90007, USA 


AND 


W. P. POPENOE! 


University of California, Los Angeles 


Abstract. 


Eighteen species of Pacific Slope Turonian (Late Cretaceous) gastropods are discussed. 


Nine of the species and six of the genera are new. The new genera are Praesargana, Cydas, Saturnus, 
Skyles, Varens, and Konistra. The new species are Anchura (Helicaulax) tricosa, Confusiscala? yuvenca, 
Confusiscala? sulfurea, Eripachya vaccina, Drilluta sicca, Skyles salsus, Remera vacca, Varens anae, 
and Varens formosus. The Turonian age of Palaeatractus crassus Gabb, 1869, and Saturnus dubius 
(Packard, 1922) is demonstrated. Supraspecific assignment, age, and geographic distribution of Anchura 
(Helicaulax) condoniana (Anderson, 1902), Praesargana condom (White, 1889), Cydas crossi (Anderson, 
1958), Drilluta jacksonensis (Anderson, 1958), Carota dilleri (White, 1889), Carota? mitraeformis (Gabb, 
1869), and Konistra biconica (Anderson, 1958) are discussed. Recognition of Gulf Coast and Western 
Interior genera Drilluta, Remera, and Carota for the first time in Pacific Slope faunas adds to the 
probability of greater interchange than previously recognized between the Gulf Coast-Western Interior 


and the Pacific Slope during the Turonian. 


INTRODUCTION 


Pacific Slope molluscan faunas of Cretaceous age remain 
underdescribed. W. P. Popenoe worked on the rich Cre- 
taceous fauna of the Redding area, Shasta County, Cali- 
fornia (Figure 1), for roughly 50 years. He was particu- 
larly interested in gastropods of Turonian age and left at 
his death unpublished descriptions of a number of species. 
This paper describes or discusses 18 species, nine of which 
are new, and proposes six new genera. Although these 
descriptions are from an uncompleted manuscript on the 
Redding area, not all of the specimens discussed are from 
there. Figure 1 is an orientation map for places of occur- 
rence. New taxa proposed are: Anchura (Helicaulax) tri- 
cosa sp. nov., Confusiscala? juvenca sp. nov., Confusiscala? 
sulfurea sp. nov., Praesargana condom (White, 1889) gen. 
nov., Cydas cross: (Anderson, 1958) gen. nov., Eripachya 
vaccinus sp. nov., Saturnus dubius (Packard, 1922) gen. 
nov., Drilluta sicca sp. nov., Skyles salsus gen. et sp. nov., 


' Deceased. 


Remera vacca sp. nov., Varens anae gen. et sp. nov., Varens 
formosus gen. et sp. nov., and Konistra biconica (Ander- 
son, 1958) gen. nov. Systematic and stratigraphic position 
and geographic distribution are discussed for Anchura 
(Helicaulax) condoniana Anderson, 1902, Palaeatractus 
crassus Gabb, 1869, Drilluta jacksonensis (Anderson, 1958), 
Carota dillerr (White, 1889), and Carota? mutraeformis 
(Gabb, 1869). Palaeatractus crassus Gabb, 1869, “‘Cordi- 
era” mitraeformis Gabb, 1869, Acteon politus Gabb, 1869, 
and Liocium punctatum Gabb, 1869, were originally de- 
scribed “From the Shasta Group, from a canyon in the 
foothills, a mile south of the road from Colusa to the 
Sulphur Springs near the eastern margin of the Coast 
Range, Colusa County,” and considered by GaBB (1869) 
to be of Early Cretaceous age. All four have, however, 
been collected from beds of Turonian age in the Redding 
Formation. 

Pacific Slope Cretaceous gastropod faunas show, in gen- 
eral, little similarity to faunas of the Gulf Coast and West- 
ern Interior, but generic affinities of the Pacific Slope Seno- 
nian gastropods to those of Japan have commonly been 


Page 352 


The Veliger, Vol. 36, No. 4 


recognized. However, among the 13 Turonian genera dis- 
cussed in this paper, four are also present in the Gulf 
Coast-Western Interior and a fifth, Praesargana, bears 
strong resemblance to a Gulf Coast genus. These gastro- 
pods thus suggest greater interchange with Atlantic realm 
faunas during the Turonian than during the Senonian. 
Quantitative comparisons of these faunas must await more 
complete description of the Pacific Slope faunas. In ad- 
dition to increasing the knowledge of the paleogeographic 
distributions of some groups, the descriptions of these Tu- 
ronian forms increase our ability to assess biodiversity of 
the past. 

Curatorial abbreviations used are CASG = California 
Academy of Sciences, Geology; CIT = California Institute 
of Technology; CSMB = California State Mining Bureau; 
GSC = Geological Survey of Canada; LACM = Natural 
History Museum of Los Angeles County, Malacology Sec- 
tion; LACMIP = Natural History Museum of Los An- 
geles County, Invertebrate Paleontology Section; MCZ = 
Harvard University, Museum of Comparative Zoology; 
UCBMP = University of California, Berkeley, Museum 
of Paleontology; UCLA = University of California, Los 
Angeles, Department of Earth and Space Sciences; UCR 
= University of California, Riverside, Department of Geo- 
logical Sciences; USGS = United States Geological Survey; 
USNM = United States National Museum; UW = Uni- 
versity of Washington, Thomas Burke Museum. 

In the following descriptions, species characterized as 
small are under 20 mm in height; those characterized as 
medium-sized range between 20 mm and 60 mm in height; 
and those characterized as large are 60 mm or more in 
height. 

Features measured are listed by the following abbre- 
viations in tables: height = H; maximum diameter = D; 
height of penultimate whorl = Hp; diameter of penulti- 
mate whorl = Dp; height of spire = Ha; height of shoulder 
on penultimate whorl = Hs; length of extended outer lip 
in aporrhaids = Lw; length of prong in aporrhaids = Lp; 


Figure 1 


Index map. Two sequences have provided the bulk of the studied 
material: the exposures of the Redding Formation, northeast of 
Redding, Shasta Co., and the lower part of the Ladd Formation 
in the northern Santa Ana Mountains, Orange Co., California. 
A third significant unit is the Osburger Gulch Member of the 
Hornbrook Formation cropping out in Jackson Co., Oregon, and 
Siskiyou Co., California. Place names (starred) mentioned in the 
text are: 1, Antelope Valley, Kern. Co., California; 2, Cedros 
Island, Baja California, Mexico; 3, Colusa to the Sulphur Springs, 
Colusa Co., California; 4, Martinez, Contra Costa Co., Califor- 
nia; 5, Phoenix, Jackson Co., Oregon; 6, Redding, Shasta Co., 
California; 7, Santa Ana Mts., Orange Co., California; 8, Sis- 
kiyou Co., California; 9, Simi Hills, Los Angeles Co., California; 
10, Sucia Island, San Juan Co., Washington; 11, Sydney Island, 
Straits of Georgia, British Columbia; 12, Tuscan Springs, Te- 
hama Co., California. 


L. R. Saul & W. P. Popenoe, 1993 


length of aperture = La; length of rostrum = Lr; pleural 
angle = A; number of axial ribs per whorl = R. 


SYSTEMATIC PALEONTOLOGY 
Phylum Mollusca Linnaeus, 1758 
Class Gastropoda Cuvier, 1797 
Order Mesogastropoda Wenz, 1938 
Superfamily Strombacea Rafinesque, 1815 
Family APORRHAIDAE Gray, 1850 


Aporrhaids have an aperture with at least three large sinus 
areas that are independent of the lip extensions. One is 
posterior and adjacent to the whorl, the second bends the 
outer lip next to the rostrum, and the third is a hollow 
across the base of the columella and whorl! base that exits 
on the body side of the anterior rostrum. When the animal 
is in living position, these sinuses accommodate the head 
and foot of the animal beneath the shell (Figure 2). The 
depth of the basal sinus (Figure 2C) is accentuated in some 
aporrhaids by the buildup of callus on the apertural face 
of the last whorl. In Campanian and Maastrichtian An- 
chura spp. these calluses are commonly very thick, but in 
the Turonian Helicaulax spp. the inner lip is thin to thick 
and not expanded onto the face of the last whorl. 


Genus Anchura Conrad, 1860 


Type species: Anchura abrupta Conrad, 1860, by monotypy, 
from the Gulf Coast Maastrichtian. 


Diagnosis: Medium- to large-sized aporrhaids with high, 
evenly tapering spires; sculpture ornate, with both axial 
and spiral elements, commonly noded at intersections; ap- 
erture sublenticular; anterior rostrum long and narrow; 
outer lip elongate, extended into a falcate digitation, bent 
posteriorly. 


Subgenus Anchura Conrad, 1860 


Diagnosis: Anchura with the long narrow anterior rostrum 
deflected to the left in apertural view; lateral arm of the 
outer lip without flanges. 


Discussion: Time and geographic ranges of the subgenus 
Anchura are difficult to determine in the absence of more 
complete studies of various species that have been assigned 
to it (SOHL, 1960). The subgenus is well represented in 
beds ranging in age from Cenomanian through Maastrich- 
tian of North America and Europe. It appears to have a 
longer range and be more prolific in the Western Interior 
and the Gulf Coast than elsewhere. On the Pacific Slope 
it has not yet been found earlier than Turonian. Two 
Pacific Slope species have been described, Anchura (An- 
chura) falciformis (Gabb, 1864) of early Campanian age 
and A. (A.) gibbera Webster, 1983, of early Maastrichtian 
age. Although “Anchura” angulata (Gabb, 1864) of ?Al- 


Page 353 


Figure 2 


Three large sinus areas of the aporrhaid aperture. A. Posterior 
sinus to accommodate the posterior part of the foot. B. Anterior 
outer lip sinus to accommodate the snout. C. Basal sinus to 
accommodate the anterior part of the foot. (Example is modern 
Aporrhais pespelecani (Linnaeus, 1758) from the Mediterranean 
Sea, LACM 149737x (= UCLA cat. no. 41586). 


bian—Cenomanian age resembles Anchura in overall shape, 
it has a wing more like that of Drepanochilus Meek, 1864, 
or Dimorphosoma Gardner, 1875, and very fine sculpture 
on the spire that is distinctly different than the ornate 
sculpture of typical Anchura. 


Subgenus Helicaulax Gabb, 1868 


Type species: Rostellaria ornata d’Orbigny, 1843, by subse- 
quent designation (COSsMANN, 1904), from the Turo- 
nian of France. 


Diagnosis: Medium-sized, high-spired aporrhaids with 
whorls ornately sculptured by both axial and spiral ele- 
ments and usually noded at the intersections; last whorl 
uniangulate; anterior rostrum elongate, narrow, straight; 
aperture subquadrate; posterior digitation reflexed, elon- 
gate, and adnate to spire at its base; outer lip extended, 
falcate, tapering posteriorly to a spike; inner lip thin to 
thick. 


Discussion: Helicaulax resembles Anchura Conrad, 1860, 
in spire, sculpture, rostrum, and expansion of the outer 
lip, but it differs from Anchura in having, in addition to 
its expanded outer lip, an elongate, reflexed posterior dig- 
itation that is adnate to the spire (SOHL, 1960:103). In 
typical Anchura the anterior rostrum is deflected to the left 
in apertural view, but in Helicaulax it is straight. Helicaulax 
tends to develop flanges along the lateral segment of the 
outer lip. Although GaBB (1868), when proposing the sub- 
genus, placed two California species, in addition to the 
type species, in Helzcaulax, neither of these California spe- 
cies can be retained in it (SOHL, 1960). Helicaulax bicarina- 
ta Gabb, 1864, of ?Albian age, is a Tessarolax Gabb, 1864, 
and H. costata Gabb, 1864, of Paleocene age is, according 
to STEWART (1927), an Araeodactylus Harris & Burrows, 
1891. The chronologic range of Helicaulax is Cenomanian 
to Maastrichtian (SOHL, 1960). Anchura (Helicaulax) con- 
domiana and A. (H.) tricosa are the only known Pacific 
Slope representatives of this subgenus, which is better 
known from the Western Interior and Gulf Coast of North 
America and from Europe. Whereas Anchura (Anchura) 
is more common in North American Upper Cretaceous 
deposits, A. (Helicaulax) is better represented in Europe. 


Page 354 


Both A. (H.) condoniana and A. (H.) tricosa differ from 
the typical European forms in having the posterior digi- 
tation that sprouts adjacent to the whorl, thereafter un- 
attached rather than adnate for part of its length. Addi- 
tionally, the inner lip of these West Coast species is thick 
whereas that of A. (H.) ornata is very thin (COSSMANN, 
1904:64). Helicaulax has been considered a subgenus of 
Aporrhais da Costa, 1778, by COSSMANN (1904) and WENZ 
(1940), but it differs from Aporrhais in having a laterally 
extended falcate outer lip that tapers to a spike rather than 
the broadly palmate digitated wing of Aporrhais. In Apor- 
rhais the ornamentation tends to have a bicarinate orien- 
tation, but on Helicaulax and Anchura the complex sculp- 
ture has axial and spiral elements that commonly form 
nodes at intersections. On the last whorl, one or two of 
the spirals increase in strength to give the body whorl an 
unicarinate profile. Although Helicaulax differs from An- 
chura in having (1) a posterior digitation, (2) flanges along 
the lateral extension of the wing, (3) a straight anterior 
rostrum, Helicaulax is so similar to Anchura Conrad, 1860, 
that the two must be closely related. Of the two Pacific 
Slope species, Anchura (Helicaulax) condoniana has more 
poorly developed flanges along the wing and a shorter 
posterior prong that is late to develop and then callused 
over. It appears, thus, to be more similar to Anchura than 
is A. (H.) tricosa. Except for its posterior digitation and 
straight anterior rostrum, A. (H.) condoniana is similar to 
Anchura. SOHL (1960:106) gives the range of Anchura as 
Cenomanian through Maastrichtian, and includes Anchura 
turricula Stephenson, 1952, from the Cenomanian age 
Woodbine of Texas despite its slight flanges on the lateral 
extension of the wing. The morphologies of both A. (H.) 
condoniana and A. turricula appear transitional between A. 
(Helicaulax) and A. (Anchura). 

The two Pacific Slope Turonian species of Anchura 
(Helicaulax) have different known geographic and sedi- 
ment distributions. Anchura (H.) condoniana has a more 
northern distribution in sandstone; A. (H.) tricosa has a 
more southern distribution in siltstone. Some of the mor- 
phological features of A. (H/.) tricosa, especially the long 
posterior prong and the expanded flanges on the lateral 


The Veliger, Vol. 36, No. 4 


extension of the wing, seem appropriate to a quiet-water 
habitat on a fine-grained substrate, and the retrieval of 
these two species from different sediment types is probably 
related to their ecologic preferences. At present, the sig- 
nificance of the north-south distributions of these two spe- 
cies cannot be determined. 


Anchura (Helicaulax) condoniana (Anderson, 1902) 
(Figures 3-18) 


Anchura condoniana ANDERSON, 1902:76, pl. 8, fig. 179; JONES, 
SLITER & POPENOE, 1978:xxii.9, pl. 1, fig. 15. Not An- 
chura condoniana Anderson of STADUM, 1973, cover pho- 
to = A. (H.) tricosa sp. nov. 

Drepanochilus condoniana (Anderson): ANDERSON, 1958:166. 


Diagnosis: A Helicaulax having a short posterior digitation 
roughly parallel to the shell axis, adjacent to the spire at 
its base, but not otherwise adnate; sculpture dominantly 
axial; fifth and sixth abapical spiral cords forming the 
angulation and continuing onto extended outer lip; outer 
lip falcate but only slightly flanged posteriorly and ante- 
riorly along its lateral portion. 


Description: Shell medium sized, high spired, turriculate, 
drawn out anteriorly into a moderately long, nearly straight 
anterior rostrum; whorls about eight in number, barely 
convex; suture appressed; protoconch unknown; growth 
line antispirally concave on the spire. Sculpture ornate, 
consisting of axial and spiral elements, the axial dominant 
on whorl sides; surface of spire ornamented by about 20 
slightly arcuate axial ribs crossed by six spiral ribs forming 
nodes at axial-spiral intersections; the first four abapical 
ribs separated by interspaces of nearly equal width, the 
fifth, sixth, and seventh closer together, the fifth and sixth 
forming the peripheral angulation on the last whorl and 
continuing onto the extended outer lip. Aperture subquad- 
rate, deeply broadly sinused between posterior spur and 
falcate digitation; outer lip with two extensions, a short 
straight, spurlike process adjacent to the spire and a long 
and falcate digitation, slightly flanged both posteriorly and 
anteriorly along its lateral portion, and grooved internally 


Explanation of Figures 3 to 18 


All figures x1; all specimens, except LACMIP cat. no. 11537, 
coated with ammonium chloride. 


Figures 3-10. Anchura (Helicaulax) condoniana Anderson, 1902. 
Figure 3: LACMIP cat. no. 10837 from UCLA loc. 4214, ho- 
lotype, apertural view. Figure 4: CAS cat. no. 445.30 from CAS 
loc. 445, holotype, back view. Figures 5-8: LACMIP cat. no. 
11540 from LACMIP loc. 10735, hypotype; Figure 5, right side; 
Figure 6, back; Figure 8, aperture. Figure 7: LACMIP cat. no. 
11539 (latex pull) from LACMIP loc. 10735, hypotype, aperture. 
Figure 9: LACMIP cat. no. 11537 (latex pull) from LACMIP 
loc. 10726, hypotype, back, apparent bend in rostrum results 
from imperfection in rock mold. Figure 10: LACMIP cat. no. 
11538 from UCLA loc. 4214, hypotype, back. 


Figures 11-18. Anchura (Helicaulax) tricosa sp. nov. Figure 11: 
USNM cat. no. 465514 from USGS loc. 2759, holotype, aperture. 
Figure 12: USNM cat. no. 465515 from USGS loc. 2759, para- 
type, back. Figure 13: Paratype, USNM cat. no. 465518 from 
USGS loc. 2757, back. Figures 14, 15: USNM cat. no. 465517 
from USGS loc. 2757, paratype; Figure 14, aperture; Figure 15, 
back. Figure 16: UCR cat. no. 7787/101 from UCR loc. 7787, 
paratype, aperture. Figure 17: LACMIP cat. no. 11541 from 
UCLA loc. 4235, paratype, back. Figure 18: Chapman College 
specimen figured by STADUM (1973) from Ladd Formation, up- 
per Holz Shale Member, Santa Ana Mts., California, paratype, 
collected and prepared by Frank and Mabel Grouard. Photo- 
graphs 3, 9, 10, 18 by Susuki; 4-8, 11-17 by De Leon. 


L. R. Saul & W. P. Popenoe, 1993 Page 355 


The Veliger, Vol. 36, No. 4 


Table 1 


Measurements (mm) of Anchura (Helicaulax) condoniana Anderson, 1902. 


CAS 445.30 45.0* 23.0 9.0 16.4 


Page 356 

H D Hp Dp 
UCLA 58437 58.7* 17.0t 6.4 14.6t 
LACMIP 11537e 42.8* 17.4 7.8 14.8 
LACMIP 11538 41.5* 19.0+ 7.0 15.0t 
LACMIP 115390 46.0* —_ = — 
LACMIP 11540 60.0 = 7.0 = 


Ha Lw Lp A Lr Dp/Hp 
25.0 — — 34° — 1.8 
18.0* 30.0* = 39° 24.0 DS 
23.0* — — 352 — 1.9 
22.8* — — 36° = 2.1 
29.0 31.0 11.0 30° — 

2515 26.0 19.0 


* Specimen incomplete; ¢ specimen crushed; @ latex pull. Abbreviations decrypted in Introduction. 


opposite the external ridge; groove filled by thick callus 
deposit within aperture; inner lip very thick. 


Holotype: CASG cat. no. 445.30. 


Hypotypes: LACMIP cat. nos. 10837 (= UCLA 58437), 
11538 from LACMIP loc. 24214 (= UCLA loc. 4214), 
Little Cow Creek; 11537 from LACMIP loc. 10726 (= 
CIT loc. 1032), Dry Creek; 11539-11540 from LACMIP 
loc. 10735 (= CIT loc. 1212), Little Cow Creek, Shasta 
Co., California. 


Dimensions: See Table 1. 


Type locality: CASG loc. 445, Forty-nine mine, near 
Phoenix, Jackson Co., Oregon (Anderson, 1902). 


Distribution: Unnamed formation on Sidney Island (coll.: 
Peter Ward, 3 September 1992), British Columbia; Horn- 
brook Formation, Jackson Co., Oregon; Hornbrook For- 
mation, Osburger Gulch Member, Siskiyou Co., Califor- 
nia; Redding Formation, Bellavista Sandstone Member, 
rare, Frazier Silt Member, locally abundant, Melton 
Sandstone Member, rare, northeast of Redding, Shasta 
Co., California. 


Geologic age: Middle to late Turonian, at LACMIP loc. 
10876 (= CIT loc. 1042) associated with Subprionocyclus 
neptuni (Geinitz, 1849) (MATSUMOTO, 1960:102). 


Remarks: The holotype was rescued from the ashes after 
the 1906 San Francisco earthquake. It now lacks the ex- 
panded wing and the rostrum of ANDERSON’s (1902) figure 
(figure 179). 

The extended wing of Anchura (H.) condoniana appar- 
ently formed before the posterior prong. Several specimens 
that have an extended falcate outer lip have no posterior 
spur (e.g., the specimen figured by JONEs et al., 1978:pl. 
1, fig. 15) and no indication that one has broken off. Ap- 
ertures of specimens that have a spur have thicker callus 
deposits within the aperture, suggesting that these are more 
mature specimens. 

Anchura (Helicaulax) condoniana differs from the similar 
A. (#.) tricosa in having the prong shorter and at less of 
an angle to the shell axis, only suggestions of flanges along 


the lateral extension of the outer lip, and a sturdier shell. 
The more strongly noded sculpture of A. (H.) condoniana 
is more similar to that of typical Helzcaulax than is that 
of A. (H.) tricosa. 

PACKARD (1916:148) reported both Alaria condoniana 
and Alaria falciformis (Gabb, 1864) from the “Actaeonella 
oviformis” Zone of the Santa Ana Mountains. “‘Actaeonella 
oviformis” in the Santa Ana Mountains is T7ochactaeon 
(T.) packard: (Anderson, 1958) and of Turonian age (SOHL 
& KOLLMANN, 1985). Anchura (Helicaulax) condoniana is 
also from the Turonian, but specimens so identified from 
the Santa Ana Mountains thus far examined are Anchura 
(Helicaulax) tricosa sp. nov. POPENOE (1942:fig. 4) re- 
corded Anchura cf. A. falciformis (Gabb, 1864) from nine 
localities in the Santa Ana Mountains. The specimens from 
his localities in the Baker Canyon Sandstone and “Holz- 
Baker Transition” are also A. (H.) tricosa sp. nov. with 
the exception of those from LACMIP loc. 10100 (= CIT 
loc. 92) which are an undescribed new species of Anchura 
(Anchura). Popenoe’s specimens of A. cf. A. falciformis from 
the upper Holz Shale belong to another undescribed species 
of Anchura (Anchura). The Anchura (Helicaulax) condon- 
tana of STADUM (1973) from the Santa Ana Mountains 
Turonian is an unusually complete specimen of Anchura 
(Helicaulax) tricosa sp. nov. Anchura (Helicaulax) condon- 
zana is locally abundant in the Redding region, but few 
specimens have the rostrum and extended outer lip pre- 
served. 


Anchura (Helicaulax) Saul & Popenoe, 
tricosa sp. nov. 


(Figures 11-18) 


Anchura condoniana Anderson: STADUM, 1973, cover photo. 
Not Anchura condoniana Anderson, 1902. 


Diagnosis: A large-sized Helicaulax with a long, posterior 
prong that is at an angle to the shell axis and a falcate 
outer lip broadened both anteriorly and posteriorly by 
angulate flanges. 


Description: Shell large, high spired, drawn out anteriorly 
into a long, straight anterior rostrum; whorls about nine 


L. R. Saul & W. P. Popenoe, 1993 


Table 2 


Measurements (mm) of Anchura (Helicaulax) tricosa sp. nov. 


LACMIP 11541 53.0* 19°77 Poll 14.3 


H D Hp Dp 
LACMIP 11542 43.7* 19.5 8.8 15.8 
UCR 7787/101 52a 17.07 7.5 14.7 
USNM 465514 42.0* 16.5 6.8 1325 
USNM 465515 50.0* 18.0 6.7 12.0 
USNM 465517 37.0* 16.0 8.0 12.6 
USNM 465518 45.0* 21.0 9.0 15.8 


Page 357 
Ha Lw Lp A Lr Dp/Hp 
25.0* 31.0 22.0 30° 13.8* 1.8 
26.0* 32.5", 10.0* 25 — 1.8 
Paarl 333% 19.0 28° — 2.0 
24.0* 33.0* 14.0 206° — 2.0 
31.0 45.5* 22.0 Cds 8.0* 1.8 
15.0* 29.6* 16.0 Die _— 1.6 
19.0* Soe: 14.5* — 10.0* 1.8 


* Specimen incomplete; + specimen crushed. Abbreviations decrypted in Introduction. 


in number, wider than high, barely convex; suture im- 
pressed; body whorl angulate; anterior rostrum longer than 
the last whorl, slender, straight; early whorls with arcuate 
axial ribs; penultimate whorl ornamented by about 16 
axial ribs crossed by straplike spiral ribs, about five on the 
spire and eight or nine on the body whorl; ribs forming 
nodes at intersections; first three abapical ribs separated 
by slightly wider interspaces, fourth and fifth closer to- 
gether, forming the angulation of the body whorl that 
extends onto the outer lip digitation. Aperture subtrian- 
gular, deeply broadly sinused between posterior spur and 
falcate digitation; outer lip with two extensions, a relatively 
long, straight, spurlike posterior process basally adjacent 
to the spire and a long, and falcate digitation flanged both 
posteriorly and anteriorly along its lateral extension; pos- 
terior prong at an angle of 20°-30° to the shell axis. 


Holotype: USNM cat. no. 465514. 


Paratypes: LACMIP cat. nos. 11541 from UCLA loc. 
4235, Holz Ranch, and 11542 from LACMIP loc. 15295, 
Silverado Canyon, Santa Ana Mts., Orange Co., Califor- 
nia; UCR cat. nos. 7787/101, from UCR loc. 7787, Sil- 
verado Canyon, and 7788/20, from UCR loc. 7788, Sil- 
verado Canyon, Santa Ana Mts., Orange Co., California; 
USNM cat. nos. 465517-465518 from USGS loc. 2757, 
Silverado Canyon; USNM eat. nos. 465515-465516 from 
USGS loc. 2759, Ladd Canyon, Santa Ana Mts., Orange 
Co., California; Stadum specimen. 


Type locality: USGS loc. 2759, lower Ladd Canyon, near 
Silverado Canyon, Santa Ana Mts., Orange Co., Califor- 
nia. 


Dimensions: See Table 2. 


Distribution: Ladd Formation, upper Baker Canyon 
Sandstone and lower Holz Shale members, uncommon, 
Santa Ana Mts., Orange Co., California. 


Geologic age: Turonian. 


Remarks: Anchura (Helicaulax) tricosa differs from A. 
(H.) condoniana in having a broader falcate outer lip with 


angulately developed flanges, a longer posterior spur that 
extends at a greater angle to the shell axis, fewer axial 
ribs on the spire, a narrower pleural angle, and a slightly 
taller spire. On most available specimens, both axial and 
spiral sculpture appear more subdued than on A. (/.) 
condoniana, but this is at least partly due to preservation. 
A few specimens (e.g., the holotype and paratypes UCR 
7788/101-102) have the sculpture fairly well preserved. 
On these A. (H.) tricosa, the spirals are narrower and the 
interspirals wider, the axials fewer, and the nodes at the 
intersection stronger, especially on the angulation, than on 
A. (H.) condoniana. Anchura (H.) tricosa is from fine- 
grained muddy sandstone and siltstone, but A. (H.) con- 
doniana is common in beds of coarser grain. A fragmentary 
specimen (USNM cat. no. 465516) of A. (H.) tricosa has 
a body whorl diameter of about 20 mm, suggesting a height 
of at least 72 mm, a size close to twice that of any A: (H.) 
condoniana. As discussed under A. (H.) condoniana, PACK- 
ARD’s (1916) Alara condoniana from the Santa Ana Moun- 
tains is Anchura (H.) tricosa as is POPENOE’s (1942) 
Anchura cf. A. falciformis from the upper Baker Canyon 
Sandstone and lower Holz Shale members of the Ladd 
Formation. POPENOE’s (1942) specimens of A. cf. A. fal- 
ciformis from the upper Holz Shale differ from A. (H.) 
tricosa in lacking the posterior prong, in having a shorter 
lateral extension to the wing that lacks flanges, and in 
being more coarsely sculptured. USNM 465515 was en- 
crusted with calcareous tubes (probably annelid) on both 
apertural and abapertural sides of the wing and on the 
base of the body whorl adjacent to the lip. These encrusta- 
tions were probably subsequent to the death of the gas- 
tropod. 


Etymology: The species name is from the Latin tricosus, 
meaning full of tricks or wiles. 
Superfamily ? JANTHINACEA, Lamarck, 1812 
Family EPITONIIDAE Berry, 1910 


SOHL (1964) placed the Epitoniidae in the order Cephalas- 
pidea, but PONDER & WAREN (1988) have included it in 


Page 358 


Explanation of Figures 19 to 26 


All figures x1; all specimens coated with ammonium chloride. 


Figures 19-24. Confusiscala? sulfurea sp. nov. Figures 19, 20: 
CAS cat. no. 66549.01 from CAS loc. 66549, holotype; Figure 
19, aperture; Figure 20, back. Figures 21, 22: LACMIP cat. no. 
11544 from UCLA loc. 7233, paratype; Figure 21, apertural 
side; Figure 22, back. Figures 23, 24: LACMIP cat. no. 11545 
from UCLA loc. 4252, paratype; Figure 23, aperture; Figure 
24, back. 


Figures 25, 26. Confusiscala? juvenca sp. nov. Figures 25, 26: 
LACMIP cat. no. 11543 from LACMIP loc. 10735, holotype; 
Figure 25, apertural side; Figure 26, back. Photographs, 19-24 
by De Leon; 25, 26 by Susuki. 


the superfamily Janthinoidea, Lamarck, 1812, which they 
place near the end of the Mesogastropoda. 


Genus Confusiscala de Boury, 1909 


Type species: by original designation and monotypy, Scalaria 
dupiniana d’Orbigny, 1842, from Aube, France, of Al- 
bian age. 


Confusiscala was originally considered to be a subgenus 
of Amaea by DE Boury (1909). It has continued to be 
treated as a subgenus by several workers, including STEW- 
ART (1927), who placed it as a subgenus of Epitonium 
Roding, 1798, WENz (1940) as a subgenus of Amaea H. 
& A. Adams, 1853, and DURHAM (1937) as a subgenus 
of Opalia H. & A. Adams, 1853. GARDNER (1876) had 
included Scalaria dupiniana and its allies in Opalia, and 


The Veliger, Vol. 36, No. 4 


the two species described here resemble Opalia. Confusis- 
cala? juvenca is as similar to Opalia as to Confusiscala. 

COssMANN (1912:73) considered Confusiscala a full ge- 
nus and characterized it as having axial ribs and varices 
that do not cross the basal cord, which is visible on the 
spire supradjacent to the suture. The axial ribs are not 
always aligned with ribs of adjacent whorls, and they are 
posteriorly somewhat reflected toward the basal cord. Whorl 
sides are completely overrun by fine spiral threads. The 
base is rather flat and circumscribed peripherally by the 
somewhat projecting basal cord against which the axial 
ribs abut. The basal disk is ornamented by fine spiral 
threads and crossed by radiating slightly sinuous growth 
lines. The aperture has a small posterior canal against the 
basal cord of the penultimate whorl. 

COssMANN (1912) listed occurrences of species referred 
to Confusiscala from nearly all continents, but the genus 
has apparently not been recognized in the Western Inte- 
rior, Atlantic, and Gulf Coast Cretaceous faunas of the 
United States. The genus ranges from Neocomian (GARD- 
NER, 1876) through Maastrichtian. 


Confusiscala? sulfurea Saul & Popenoe, sp. nov. 
(Figures 19-24) 


Opalia (Confusiscala) mathewsonu (Gabb)?: DURHAM, 1937: 
504, pl. 56, fig. 23. 


Diagnosis: A medium-sized Confusiscala with axial ribs 
that extend from suture to basal cord and increase grad- 
ually in number, 12 on the fifth whorl and 19 on the 12th 
whorl; basal cord variably exposed on spire. 


Description: Shell medium sized, turreted; pleural angle 
about 24°; whorls 12, moderately convex, width more than 
twice height; sutures impressed, not always anterior to the 
basal cord; basal disk flattened, bordered peripherally by 
a strong cord and centrally by a low swelling about an 
indistinct umbilical depression. Whorl sides sculptured by 
strong, scarcely sigmoid, swollen, round crested axial ribs, 
overridden by fine spiral threads; ribs just reaching the 
posterior suture and terminating at the basal cord, nearly 
aligned with ribs of adjacent whorls, but not confluent, 12 
ribs on fifth whorl, 19 ribs on twelfth whorl; rib interspaces 
round bottomed, about equal in width to the ribs; spiral 
sculpture of low, spaced, spiral threads of alternating 
strength; base with fine more closely spaced nearly equal 
spiral threads; growth line a little prosocline at the suture, 
broadly barely concave medially. Aperture subquadrate; 
inner lip narrow, a little thickened. 


Holotype: CASG cat. no. 66549.01 (= CASG cat. no. 
7010, DURHAM, 1937:pl. 56, fig. 23) 


Paratypes: LACMIP cat. no. 11545 from UCLA loc. 
4252, Ashland, Oregon; and 11544 from UCLA loc. 7233, 
Sulphur Creek, Redding quadrangle, Shasta Co., Cali- 
fornia. 


L. R. Saul & W. P. Popenoe, 1993 


Dimensions: See Table 3. 


Type locality: CASG loc. 66549, Hagerdorn Ranch, 4 
miles (6.4 km) northwest of Montague, Siskiyou Co., Cal- 
ifornia. 


Distribution: Hornbrook Formation, ?Osburger Gulch 
Member, near Ashland, Jackson Co., Oregon; Hornbrook 
Formation, ?Osburger Gulch Member, near Montague, 
Siskiyou Co.; Redding Formation, Bellavista Sandstone 
Member, Redding area, Shasta Co., California. 


Geologic age: Turonian. 


Remarks: Three species resembling Confusiscala have been 
described from the Pacific Slope Cretaceous faunas. The 
first of these, ““Scalaria”’ mathewsoni Gabb, 1864, was re- 
ferred to Confusiscala by STEWART (1927). It is based on 
a single, poorly preserved specimen consisting of four in- 
complete, partially exposed whorls, from “near Martinez,” 
Contra Costa Co., California. Deposits “near Martinez” 
range in age from Albian to Maastrichtian. Preservation 
of the holotype of “S.” mathewsonu suggests that it is of 
Maastrichtian age. In C.? sulfurea the basal cord is less 
strong, the whorls are less convex, and the axial ribs are 
narrower with comparatively wider interspaces. If STEW- 
ART’s (1927) estimate that C.? mathewsonu had about 12 
axial ribs is correct, C.? sulfurea has the greater number 
of ribs. 

The second species is Mesostoma (?) newcombu Whi- 
teaves, 1903, from the Cedar District Formation of Sucia 
Island, San Juan Co., Washington. It is Campanian in 
age and differs from Confusiscala? sulfurea in its much 
larger size and relatively shorter whorl height. In C. new- 
combu axial ribs fade toward the posterior suture, creating 
a whorl profile that is broadest near its base, whereas C.? 
sulfurea has longer ribs and a more evenly rounded whorl 
profile. 

The third and even larger species is Cerithium suciense 
Packard, 1922, described from a specimen consisting of 
two whorls (height 59 mm, diameter 44 mm) probably 
from the Cedar District Formation on Sucia Island, San 
Juan Co., Washington (UCB loc. 2209), which is of mid 
Campanian age. Another and larger specimen consisting 
of eight whorls (height incomplete 162 mm, diameter 56 
mm) is available from that part of the Chatsworth For- 
mation in the Simi Hills yielding Metaplacenticeras aff. M. 
pacificum (Smith, 1900). Confusiscala suciense is from the 
Hoplitoplacenticeras vancouverense to Metaplacenticeras pa- 
cificum zones and of mid to late Campanian age. Confus- 
iscala? sulfurea is much smaller than C. suciense and lacks 
the strong posterior growth line sinus just subjacent to the 
suture. 

The holotype of Confusiscala? sulfurea was described 
as being “from the upper Chico beds,” reflecting common 
usage 60 years ago, but the Cretaceous strata near Monta- 
gue are now referred to as the Hornbrook Formation. 
Present in the matrix of the holotype are specimens of 


Page 359 


Table 3 


Measurements (mm) of Confusiscala ? sulfurea sp. nov. and 
C.? guvenca sp. nov. 


H D Hp Dp A R Hp 
C.? sulfurea 
CASGI66549:01) 5751-3) 1\9)0) 93825) 94:40 22?) 19) Ae7 
LACMIP 11544 45.8 14.6f 7.5 OFA Ie ile Sey le? 
LACMIP 11545 27.2 125 5.6 10.5 26° 13 1.9 
C.? juvenca 
LACMIP 11543 27.4 10.9 50 8.9 SIO Aes 


* Specimen incomplete; ¢ specimen crushed. Abbreviations de- 
crypted in Introduction. 


Turntella hearni Merriam, 1941, a species of Turonian 
age that is present in the lower Hornbrook Formation. 

Confusiscala? sulfurea is not a typical Confusiscala. Its 
axial ribs, like those of C.? mathewsoni, extend from the 
posterior suture to the basal cord, and it differs from C. 
dupiniana in having longer axial ribs and a more evenly 
rounded whorl profile. 


Etymology: The species name sulfurea is Latin and refers 
to the occurrence of this species on Sulphur Creek, Shasta 
Co., California. 


Confusiscala? guvenca Saul & Popenoe, sp. nov. 
(Figures 25, 26) 


Diagnosis: An Opalia-like epitoniid with 10 to 12 strong, 
shouldered axial ribs per whorl and a strong basal disk; 
whorls overlain with fine cancellate sculpture produced by 
fine spiral threads and growth lines. 


Description: Shell of medium size, turreted; pleural angle 
about 30°; whorls eight or nine in number, moderately 
convex, width about twice height; sutures deeply im- 
pressed; basal disk flattened, a little concave, bordered 
peripherally by a thick and rounded cord; no umbilicus. 
Whorl sides sculptured; axial sculpture of 10 to 12 nearly 
straight, slightly oblique, swollen, round-crested ribs, 
shouldered at the posterior suture, abruptly terminating 
at the basal cord, and nearly or quite in alignment with 
the ribs of adjacent whorls, but not confluent; rib inter- 
spaces round bottomed, equal in width to the ribs; spiral 
sculpture of low, faint, rather widely spaced spiral threads 
alternating with finer spiral threads and crossed by growth 
lines producing an overall finely cancellate appearance, 
extending over the basal disk; growth line with a shallow 
(about equal to % the axial rib thickness) but well-marked 
sinus at the shoulder. Aperture probably almost quadrate 
with a spoutlike extension at its inner anterior border and 
a posterior notch at the shoulder; inner lip thin, narrow, 
reflected onto base; outer lip unknown. 


Page 360 


Holotype: LACMIP cat. no. 11543. 
Dimensions: See Table 3. 


Type locality: LACMIP loc. 10735 (= CIT loc. 1212), 
Little Cow Creek, 2 miles (3.2 km) NE of Frazier Corners, 
Shasta Co., California. 


Distribution: Redding Formation, Frazier Siltstone 
Member, Redding area, Shasta Co., California. 


Geologic age: Turonian. 


Remarks: Confusiscala? yuvenca differs from C.? sulfurea 
in having strongly shouldered and straighter axial ribs, 
fewer, more irregular spirals on its basal disk, a posterior 
growth line sinus, and the suture posterior to the basal 
cord so that the basal cord does not show on the spire. In 
C.? guvenca the growth line has a posterior notch like that 
of C. suciensis, but the ribs are much straighter and longer, 
extending from the shoulder to the basal cord without 
diminished strength. 

Confusiscala? guvenca has many of the characteristics of 
the genus Opalia (type species Opalia australis (Lamarck, 
1822)), but differs in at least two respects: C.? juvenca 
has a well-marked but shallow posterior sinus to the growth 
line at the shoulder, and C.? guvenca apparently lacks the 
spiral bands of punctations of Opalia. Although the ho- 
lotype of C.? juwvenca appears well preserved, recrystali- 
zation and mineralization of the specimen may have ob- 
scured some details, and such details as punctations could 
be obscured. This species is geologically older and more 
strongly shouldered than the Maastrichtian, Gulf Coast 
species assigned to Opalia by SOHL (1964). 


Etymology: The species name juvenca is Latin, meaning 
young, and refers to the occurrence of this species in the 
Little Cow Creek drainage. 


Order NEOGASTROPODA Thiele, 1929 
Superfamily MuRICACEA Rafinesque, 1815 
Family SARGANIDAE Stephenson, 1923 


STEPHENSON (1923) proposed the new family Sarganidae 
to contain Sargana Stephenson, 1923, distinguishing it from 
Muricidae on the basis of the columellar folds and the 
flattened spire. SOHL (1964:173) and WENz (1941:1082) 
have placed Sargana in the subfamily Rapaninae of the 
family Muricidae, but PONDER & WAREN (1988) included 
Rapaninae in the Thaidinae and recognize Sarganinae. 
The placement of Sargana and of Sarganinae in Muricidae 
is questioned by GARVIE (1991), who quotes uncompleted 
work on protoconchs by Klaus Bandel as indicating that 
Sargana is a close relative of Trichotropis, and this place- 
ment was abrogated by GARVIE (1992), who places Sargana 
without attribution or mention of morphological criteria 
in the Cancellariidae. The spiny shell of Sargana does not 
resemble that of 77ichotropis. In several features—pyri- 
form shape, flattened protoconch, complex spiny sculp- 
ture—Sargana resembles Pyropsis Conrad, 1860, which 


The Veliger, Vol. 36, No. 4 


STEPHENSON (1941) placed in the Pyropsidae. SOHL (1964) 
considered the separation of the Pyropsidae as a family 
too drastic and left it in the Vasidae H. & A. Adams, 1853, 
but SAUL (1988) included Pyropsis in Tudiclidae Coss- 
mann, 1901, placing it in the superfamily Muricacea. In 
shape and placement of the posterior siphonal notch, the 
aperture of Sargana resembles that of tudiclids more than 
it does that of muricines. The aperture does not resemble 
that of trichotropids, and unlike the many muricines that 
have a posterior outer lip sinus at the shoulder rather than 
against the body whorl, the Sarganidae have a well-de- 
veloped posterior sinus against the body whorl. The ap- 
erture of Sargana also differs from that of cancellariids in 
forming a narrow, constricted anterior canal that is abrupt- 
ly confined posteriorly, whereas in cancellariids the an- 
terior canal is typically broad and not confined at its ap- 
ertural junction. 


Praesargana Saul & Popenoe, gen. nov. 
Type species: Trophon condoni White, 1889. 


Diagnosis: Small, very low-spired sarganids with mod- 
erate, lacinate anterior siphon, and a shallow umbilical 
depression bounded by a roughened fasciole. Outer lip 
bearing a tubercle opposite the spiral fold of the inner lip. 
Siphonal canal short and bent to the left. 


Discussion: Praesargana lacks the deep spiral sulcus at 
the base of the body whorl of Sargana. It has finer, more 
regular, and nodular rather than spinose sculpture; a 
smaller and shallower umbilical depression; and a shorter, 
straighter and more open siphonal canal than Sargana. 

The resemblance of Praesargana to Sargana suggests 
inclusion of Praesargana in the Sarganinae. The proto- 
conch of Praesargana is paucispiral, consisting of but two 
rapidly expanding flattened, carinate whorls. Because the 
shells are recrystallized and entombed in tenacious, well- 
cemented matrix, any fine sculpture is as yet unknown. 
In shell form and sculpture Praesargana does not resemble 
Trichotropis. Although its anterior siphonal canal is broad- 
er than that of Sargana, the anterior canal of Praesargana 
is abruptly confined posteriorly and much narrower than 
that of cancellariids. 

The generic name is compounded of Sargana, derived 
from the Greek sargane, meaning braid, plait, basket, and 
the Latin prefix Prae, meaning before, and is of feminine 
gender. 


Praesargana condoni (White, 1889) 
(Figures 27-37) 


Trophon condoni WHITE, 1889:21, pl. 3, figs. 4-5; ANDERSON, 
1958:168; JONES, SLITER & POPENOE, 1978:xxii.9, pl. 
1, figs. 8-9. 


Diagnosis: As for the genus. 


Description: Shell small; spire very low; whorls rapidly 
expanding, roundly shouldered and convex posteriorly, be- 


L. R. Saul & W. P. Popenoe, 1993 


coming concave on the short broad siphonal neck; anterior 
end of siphon rounded and lacinate; suture appressed; ramp 
slightly concave; umbilical depression shallow, narrow, 
bounded by a roughened fasciole. Protoconch paucispiral, 
consisting of about two rapidly expanding, carinate whorls 
surrounding an apical dimple. Sculpture of about 12 strong, 
evenly spaced, rough, round-topped spiral cords crossed 
by about 20 nearly straight, collabral ribs, producing a 
coarse cancellate appearance, strong at the whorl shoulder, 
diminishing anteriorly, scarcely evident on the basal fourth 
of the last whorl. Aperture broadly subovate, its two lips, 
meeting by the thickening of each as the shell approaches 
maturity, extend back upon the ultimate volution; aper- 
tural callus at posterior juncture of inner and outer lips 
bearing a shallow siphonal groove extending spireward to 
the shoulder of the penultimate whorl; aperture sharply 
constricted at its passage into anterior canal by a projecting 
tubercle on the inner margin of the outer lip, opposing a 
similarly placed spiral fold on the inner lip; siphonal canal 
short, narrow, slotlike and strongly bent to the left, margins 
parallel. 


Syntypes: USNM cat. no. 20122 (2 specimens). 


Hypotypes: LACMIP cat. no. 10807 (= UCLA cat. no. 
58443) from LACMIP loc. 10735 (= CIT loc. 1212), 
Little Cow Creek, 2 miles (3.2 km) northeast of Frazier 
Corners, Shasta Co.; LACMIP cat. no. 11546 from UCLA 
loc. 5422, Rancheria Gulch, Siskiyou Co.; LACMIP cat. 
no. 11585 from LACMIP loc. 10735 (= CIT loc. 1212), 
Little Cow Creek, Shasta Co.; LACMIP cat. no. 11586 
from UCLA loc. 4214, Little Cow Creek, Shasta Co., 
California. 


Dimensions: See Table 4. 


Type locality: “Chico Group, Little Cow Creek Valley, 
about eighteen miles [29 km] east of Redding, Shasta 
County” (WHITE, 1889). 


Distribution: Hornbrook Formation, Osburger Gulch 
Sandstone Member, Rancheria Gulch, Siskiyou Co.; com- 
mon in sandstone lenses near middle of Frazier Silt Mem- 
ber of Redding Formation, Redding area, Shasta Co., Cal- 
ifornia; reported from “Turonian of Putah Creek, near 
the Napa-Yolo County line” (ANDERSON, 1958:168). 


Geologic age: Turonian. 


Remarks: Praesargana condoni resembles Sargana stantoni 
(Weller, 1907), type species of Sargana from Maastrichtian 
of Gulf and Atlantic coasts, and S. gevers: (Rennie, 1930) 
from Senonian of Pondoland, but P. condoni lacks their 
basal constriction. Its sculpture is less spiny than that of 
S. stanton, and its protoconch is not as strongly carinate. 
It has more spiral cords on the ramp than S. geversi: and 
fewer than S. stantonz. It also resembles ““Rapana”’ tuber- 
culosa Stoliczka (1868) from the Trichinopoly beds of South 
India, but differs from this species in its more abruptly 
constricted last whorl at the beginning of the siphonal 


Page 361 


Explanation of Figures 27 to 37 


All specimens coated with ammonium chloride; unless otherwise 
indicated figures are x1. 


Figures 27-37. Praesargana condoni (White, 1889). Figures 27- 
29, 33: LACMIP cat. no. 10807 from LACMIP loc. 10735, 
hypotype; Figure 27, aperture; Figure 28, back; Figure 29, apical 
view, X 1.5; Figure 33, left side. Figures 30-32: LACMIP cat. 
no. 11546 from UCLA loc. 5422, hypotype, specimen with round- 
ed shoulder and higher spire; Figure 30, aperture; Figure 31, 
back; Figure 32, apical view, x 1.5. Figures 34, 36, 37: LACMIP 
cat. no. 11586 from UCLA loc. 4214, hypotype; Figure 34, right 
side, showing bulging portion of last whorl; Figure 36, apical 
view, higher spired specimen than 11585 (Figure 35) and 10807 
(Figures 27-29, 33). Figure 37, computer scan of Figure 34 
enhanced through use of Canvas 3.0 to show position of present 
aperture edge, varix, and former position of posterior canal, x 1.33; 
A, varix with posterior sinus; B, shoulder; C, aperture, D, um- 
bilical fasciole. Figure 35, LACMIP cat. no. 11585 from LAC- 
MIP loc. 10735, hypotype, apical view, showing suppression of 
axial ribbing and some bulging of whorl on last third of body 
whorl, x 1.5. Photographs 27, 28 by Susuki; 29-36 by De Leon. 


canal. Praesargana condonz is geologicaly older than these 
three species of Sargana. 

Praesargana condoni is morphologically variable. ‘The 
strength of the spiral cords varies from even to irregular 
with four commonly stronger, the shoulder cord and three 
alternate anterior cords (Figures 34, 37). The shoulder is 


Page 362 


The Veliger, Vol. 36, No. 4 


Table 4 


Measurements (mm) of Praesargana condoni (White, 1889). 


H D Hp 
UCLA 59443 19.0 15.0 2.0 
LACMIP 11546 27.3 RD 4.8 
LACMIP 11585 17.6 16.9 1.8 
LACMIP 11586 23.7 21.6 3.0 


Dp 


7.6 
8.9 
6.8 
10.5 


Ha Hs A Dp/Hp'  Hp/Hs 
3.0 ? 114° 3.8 ? 
6.5 1.0 88° 4.9 4.8 
3.4 E 110° 3.8 p 
5.0 iGo 52 35 1.8 


* Specimen incomplete; { shoulder overlapped. Abbreviations decrypted in Introduction. 


very angulate on some specimens but rounded on others. 
The spire height varies from nearly flat (Figures 27-29, 
33) to conical (Figures 30-32). Additionally, on some spec- 
imens an abrupt enlargement of the whorl makes a bulge 
near the aperture (Figures 34, 36, 37). 

ANDERSON (1958:168) claimed that the species occurs 
in considerable numbers near the Yolo- Napa County line 
at Putah Creek, but a search of the University of Cali- 
fornia, Berkeley, Museum of Paleontology and the Cali- 
fornia Academy of Sciences collections for specimens from 
that vicinity turned up only two specimens of the species 
from one locality, CASG loc. 2360, “Devils Gate,” on 
Berryessa Creek, 12,000 ft (3700 m) below the top of the 
Chico group, on Hamilton Ranch “near the top of the big 
conglomerate.” Anderson said that his specimens were col- 
lected from conglomerates, suggesting that Praesargana 
condoni occurs in the Venado Formation. 


Explanation of Figures 38 to 43 


All figures x1; all specimens coated with ammonium chloride. 


Figures 38-43. Cydas crossi (Anderson, 1958). Figures 38-40: 
CAS cat. no. 61934.01 from CAS loc. 61934, holotype; Figure 
38, aperture; Figure 39, back; Figure 40, right side. Figures 41- 
43: LACMIP cat. no. 11547 from LACMIP loc. 10735, hypo- 
type; Figure 41, apical view; Figure 42, apertural view showing 
pseudofold on columella; Figure 43, back. Photographs 38-41 
by De Leon; 42, 43 by Susuki. 


Superfamily BUCCINACEA Rafinesque, 1815 
Family PERISSITYIDAE Popenoe & Saul, 1987 
Genus Cydas Saul & Popenoe, gen. nov. 


Type species: Volutoderma crossi Anderson, 1958, from the 
West Coast Turonian. 


Diagnosis: Medium-sized, fusiform perissityids with a 
sloping shoulder, broadly rounded periphery, and short 
anterior siphonal neck that has near its anterior end a 
well-developed siphonal fasciole. Whorls ornamented by 
rounded axial ribs on posterior half of whorls over-ridden 
by flat-topped spiral cords. Outer lip expanded to form a 
rim and having a posterior, four medial, and an anterior 
denticle within, the central two medial denticles stronger; 
lip notched posteriorly at the shoulder between posterior 
and adapical medial denticles. Aperture elongate, narrow, 
sharply angled and constricted posteriorly. Parietal lip 
narrow and thin with one or two posterior denticles co- 
inciding with spiral cords, two pseudofolds on columella 
just anterior to base of whorl; inner lip broader and thicker 
on columella, wrapped over to form a pseudoumbilicus 
anterior to fasciole. 


Discussion: Cydas displays a typical perissityid pattern of 
apertural denticles. It is most similar to Pseudocymia Po- 
penoe & Saul, 1987, but in Cydas the outer lip denticles 
are separated into three groups and the middle two of the 
medial group are the strongest, the shoulder is obscure, 
and the spiral cords are straplike. The posterior notch at 
the shoulder of the outer lip is suggestive of Columbellaria 
Rolle, 1861, but the notch is less well developed in Cydas 
and the inner lip is not expanded onto the last whorl. 

The genus is named for Cydas of Gortyna, son of An- 
titalces, and is of masculine gender. 


Cydas cross: (Anderson, 1958) 
(Figures 38-43) 
Volutoderma crossi ANDERSON, 1958:174, pl. 16, figs. 3, 3a. 
Diagnosis: As for the genus. 


Description: Shell of medium size, rounded fusiform; spire 
and last whorl of approximately equal height; apical angle 
about 35°; spire with five, moderately convex whorls slight- 
ly concave just below suture; body whorl ornamented with 
about 12 straplike spiral cords separated by interspaces as 


L. R. Saul & W. P. Popenoe, 1993 


Table 5 


Measurements (mm) of Cydas cross: (Anderson, 1958). 


H D Hp 
CAS 61934.01 34.2* 13.9 7.0 
LACMIP 11547 33.0* 15.5 7.4 


Page 363 
Dp Ha A La Dp/Hp 
10.8 13.6* 33° 21 Ike) 
11.5 15.5 38° — i) 


* Specimen incomplete. Abbreviations decrypted in Introduction. 


wide as spirals, posterior spiral separated from posterior 
suture and succeeding abapical spiral by interspace twice 
its width; axial sculpture of about 12 low, rounded ribs 
and a varix per whorl; ribs gently arched and slightly 
concave to the aperture; varices, not well preserved in 
available specimens but developed at radial intervals of 
about 300°; aperture elongate, sharply angled posteriorly, 
contracted anteriorly; inner lip narrow, thin parietally, 
thicker and wider on columella, bearing one or two den- 
ticles near posterior end, and two short, slightly oblique 
columellar pseudofolds just anterior to whorl base; anterior 
tip of columella flexed slightly to the left, bearing a fasciole 
near its tip; outer lip expanded into a rim, bearing within 
a posterior, four medial, and an anterior denticle; two 
central medial denticles stronger; lip notched posteriorly 
at shoulder; labral profile nearly paralleling shell axis, but 
with a broad and shallow sinus concave toward the ap- 
erture. 


Holotype: CASG cat. no. 61934.01 (= CASG 10675). 


Hypotype: LACMIP cat. no. 11547 from LACMIP loc. 
10735 (= CIT 1212), Little Cow Creek, 2 miles (3.2 km) 
northeast of Frazier Corners, Shasta Co., California. 


Dimensions: See Table 5. 


Type locality: CASG loc. 61934 (= CASG 1293D), “SW 
Y% sec. 4, T32N, R3W, Frazier Corners, Shasta Co.” 
(ANDERSON, 1958). 


Distribution: Known only from the Frazier Siltstone 
Member of the Redding Formation in the vicinity of the 
type locality. 


Geologic age: Late Turonian, associated with Subprion- 
ocyclus sp. 


Remarks: Only two specimens of this species are available. 
Neither is complete; both lack an adequately preserved 
protoconch. The holotype is weathered; its shell surface is 
eroded, and the shell was riddled by endobionts, but the 
shell surface of the less complete hypotype is well pre- 
served. The aperture of the holotype is complete enough 
to display a perissityid denticle pattern. The posterior “‘si- 
phonal”’ notch is shallow, but its placement on the shoulder 
resembles the placement of the siphon in the Columbel- 
linidae. Some of the early volutes, as for example the 
species herein assigned to Carota, also have an outer lip 
notch at the shoulder. 

Cydas crossi resembles Pseudocymia aurora Popenoe & 
Saul, 1987, but C. crosst is more slender, has a less angulate 


shoulder, fewer denticles within the outer lip, and the 
denticles are more clearly divided into posterior, medial, 
and anterior groups. Cydas crossi resembles Murphitys mi- 
chaeli Saul, 1987, in overall shape but is higher spired, 
more slender, has spiral cords that are more straplike and 
regular, and has two short pseudofolds on its columella 
rather than the two folds of Murphitys. 

In shape and sculptural components, Cydas cross: re- 
sembles the type species of T7achytriton Meek, 1864, 
Trachytriton vinculum (Hall & Meek, 1856), from the late 
Campanian-early Maastrichtian of Colorado, Montana, 
South Dakota, and Wyoming. Cydas cross: differs from 7. 
vinculum in having a perissityid-like distribution of den- 
ticles within the aperture, stronger spiral sculpture con- 
sisting of fewer more nearly equal, straplike spiral cords, 
about half the number of axial ribs, and more irregularly 
developed varices, both as to strength and frequency. 


Family BUCCINIDAE Rafinesque, 1815 
Genus Eripachya Gabb, 1869 


Type species: Neptunea ponderosa Gabb, 1864, subsequent 
designation Cossmann, 1901, from the Campanian of 
California. 


Diagnosis: Medium-sized, broadly fusiform buccinids 
having plumply convex whorls; suture sinuous, impressed. 
Spiral ornamentation of alternate width ribs; collabral 
sculpture of strong, nearly straight ribs strongest at pe- 
riphery and dying out before the suture and the siphonal 
neck. Aperture eye-shaped, rounded posteriorly, attenu- 
ated and gently twisted anteriorly; siphonal canal narrow, 
moderately long; columella strongly twisted; siphonal neck 
bearing a narrow false umbilicus bounded by a low but 
well-marked fasciole; inner lip smooth, overlain by thin 
callus, concave in its parietal portion, gently sinuous in its 
columellar position; outer lip thin, lirate within. 


Range: Turonian to Campanian. 


Discussion: Eripachya has long been misunderstood. 
COssMANN (1901) indicated that it was poorly character- 
ized because the specimens were not well preserved, and 
he doubted that the other two species included by GABB 
(1869) in Eripachya, Neptunea perforata Gabb, 1864, and 
Neptunea hoffmanni Gabb, 1864, were congeneric. STEW- 
ART (1927) placed these latter species in the cancellariid 
genus Paladmete Gardner, 1916, but ANDERSON (1958) 
referred them back to Eripachya which they do not resem- 
ble. The specimen of the type species, EL. ponderosa, figured 


Explanation of Figures 44 to 54 


Unless otherwise indicated, figures are <1; all specimens coated 
with ammonium chloride. 

Figures 44-48. Eripachya vaccina sp. nov. Figures 44, 45: LAC- 
MIP cat. no. 11548, from LACMIP loc. 10760, holotype; Figure 
44, back; Figure 45, aperture. 

Figures 46-48: LACMIP cat. no. 11549, from LACMIP loc. 
10776, paratype; Figure 46, aperture; Figure 47, back; Figure 
48, apical view, x1.5. 

Figures 49-54. Eripachya ponderosa (Gabb, 1964). Figures 49, 
50, ANSP cat. no. 4186 from Tuscan Springs, Tehama Co., 
Calif., lectotype; Figure 49, back; Figure 50, aperture. Figures 
51-54: CAS cat. no. 53344.01 from CAS loc. 53344, hypotype; 
Figure 51, apical view; Figure 52, back view; Figure 53, aperture; 
Figure 54, right side. Photographs 44-47, 49, 50 by Susuki; 48, 
51-54 by De Leon. 


by STEWART (1927:pl. 20, fig. 9) is somewhat crushed into 
a less bucciniform shape. Evipachya resembles the late 
Cenozoic Lirabuccinum Vermeij, 1991, but Lirabuccinum 
has a shorter and straighter columella, more numerous 
collabral ribs, and its spiral ribbing is relatively even. The 


The Veliger, Vol. 36, No. 4 


spiral sculpture of Eripachya has a graded or bundled 
aspect with wider riblets grouped together, grading into 
finer interspace riblets somewhat like that of Kelletia kelletit 
(Forbes, 1852). 


Eripachya vaccina Saul & Popenoe, sp. nov. 
(Figures 44-48) 


Diagnosis: A slender Eripachya with about eight collabral 
ribs per whorl. 


Description: Shell of medium size, robust, broadly fusi- 
form, pleural angle of about 49°; spire approximately three- 
fifths the total height of the shell, with about six plumply 
convex whorls about twice as wide as high; siphonal neck 
slightly longer than the spire with a well-marked fasciole; 
suture undulating, slightly appressed. Protoconch un- 
known. Sculpture of fine spiral cords and strong collabral 
ribs; spiral ornamentation of five or six low, flat, narrow 
primary cords on penultimate whorl, and about 15 on body 
whorl and neck, separated by interspaces wider than the 
primaries, and alternating with narrow threadlike sec- 
ondary spirals; seven or eight sharp-crested collabral ribs 
per whorl separated by flatish interspaces, twice the width 
of the ribs; ribs on body whorl diminishing anterior to the 
periphery, not present on base or siphonal neck, disap- 
pearing at about the mid-length of whorl. Aperture eye- 
shaped, angulate at the suture, broad posteriorly, atten- 
uated anteriorly; siphonal canal narrow, of moderate length, 
twisted abaperturally and to the left anteriorly, bearing 
above its tip a narrow and shallow umbilical chink bound- 
ed by a low but well-marked fasciole; inner lip smooth, 
without folds, parietal lip short, columellar portion nearly 
straight, bent at the fasciole and with a free edge forming 
a pseudoumbilicus with the fasciole; outer lip unknown. 


Holotype: LACMIP cat. no. 11548. 


Paratype: LACMIP cat. no. 11549 from LACMIP loc. 
10776 (= CIT loc. 1197), Stinking Creek, Shasta Co., 
California. 


Type locality: LACMIP loc. 10760 (= CIT loc. 1438), 
north side Little Cow Creek, Shasta Co., California. 


Dimensions: See Table 6. 


Geologic age: ?Early Turonian, horizon of Tragodesmo- 
ceras. 


Distribution: Redding Formation, Bellavista Sandstone 
Member of the Redding area, Shasta Co., California. 


Remarks: Evipachya vaccina is a rare form; only two 
incomplete specimens are in the LACMIP collection. Both 
specimens lack a protoconch, the outer lip, and the parietal 
portion of the inner lip. Eripachya vaccina is more slender, 
has a longer anterior siphonal canal, and is ornamented 
with fewer secondary spirals than the type species, E. 
ponderosa. The holotype of E. vaccina shows no lirae on 
the outer lip but is broken back too far to be sure that lirae 


L. R. Saul & W. P. Popenoe, 1993 


were not present. Additionally the shape of the parietal 
portion of the inner lip is undeterminable, as is the presence 
of a posterior siphonal notch at the suture. 


Etymology: The specific name vaccina, Latin, meaning 
of cows, refers to the type locality on the north side of 
Little Cow Creek. 


Eripachya ponderosa (Gabb, 1864) 
(Figures 49-54) 


Neptunea ponderosa GABB, 1864:88, pl. 18, fig. 38. 

Eripachya ponderosa (Gabb): GABB, 1869:149; COSSMANN, 
1901:147, fig. 40; STEWART, 1927:425, pl. 20, fig. 9; 
WENZ, 1941:1185, fig. 3373; ANDERSON, 1958:172. 


Description: Shell of medium size, robust, bucciniform, 
apical angle of about 80°; spire approximately two-thirds 
the total height of the shell, with about six plumply convex 
whorls about twice as wide as high; suture undulating, 
and appressed; siphonal neck broad, barely longer than 
the spire, with a low well-developed fasciole. Sculpture of 
narrow spiral cords and strong collabral ribs; five or six 
primary spiral cords on penultimate whorl, 15 on body 
whorl and neck, low, flat, narrow, each bordered by graded 
sets of finer ribs; ten, moderately sharp-crested collabral 
ribs on early whorls, becoming broader, well rounded on 
body whorl, about as wide as interspaces, diminishing 
anteriorly to the periphery, disappearing on base of whorl. 
Aperture eye-shaped, broad posteriorly with a small nar- 
row posterior channel at the suture, attenuated anteriorly; 
siphonal canal moderately narrow, short, tip flexed back- 
ward and to left; inner lip smooth, without folds, parietal 
portion thin, rounded; columellar portion thicker, nearly 
straight, with a free edge forming a narrow, shallow um- 
bilical chink anterior to the fasciole; outer lip thin, lirate 
within. 


Lectotype: ANSP cat. no. 4186, here designated. 


Hypotype: CASG cat. no. 53344.01 (= CSMB cat. no. 
12793) from Tuscan Springs, Tehama Co., California. 


Dimensions: See Table 6. 


Type locality: Tuscan Springs, on Little Salt Creek, Te- 
hama Co., California. 


Distribution: A rare species, known predominantly from 
the type locality. Some small poorly preserved specimens 
from the Schultz Member of the Williams Formation in 
the Santa Ana Mountains (UCLA loc. 7199), Orange Co., 
may be this species. 


Geologic age: Campanian. 


Remarks: STEWART (1927) figured ANSP cat. no. 4186 
and referred to it as the holotype because he considered it 
to be the specimen GabB (1864) had figured. Gabb, how- 
ever, did not designate type specimens, and he mentions 
more than one specimen, but other specimens in the box 


Page 365 


Table 6 


Measurements (mm) of Eripachya vaccina sp. nov. and E. 
ponderosa (Gabb, 1864). 


Dp/ 
H D Hp Dp Ha A R Hp 
E. vaccina 
LACMIP 
11548 33.0* 17.5 6.4 11.7 12.0* 49° 8 1.8 
LACMIP 
11549 QA NALS 5:5) wn OOF 228 346 8 1.6 


E. ponderosa 


CAS 5334401 36.0* 28.7 9.0 14.6 12.0* 77° 11 1.6 
UCLA 


28733** 34.6 23.2 9.6 12.8 13.55 60°F 11 1.3 


* Specimen incomplete; + specimen crushed; ** plastercast of 
ANSP 4186. Abbreviations decrypted in Introduction. 


with Stewart’s figured specimen were “Fulgur” hilgardi 
White, 1889. Gabb did not differentiate “Fulgur” hilgardi 
from Eripachya ponderosa, and his specimens of E. pon- 
derosa from Pentz are apparently “F.” hilgardi. As STEW- 
ART (1927) did in several instances designate lectotypes, 
his reference to ANSP 4186 as holotype is an error and 
cannot be taken as designation of the lectotype. To avoid 
possible confusion, Stewart’s figured specimen ANSP 4186 
is therefore herein designated the lectotype. 

Eripachya ponderosa differs from E. vaccina in being 
stouter, having a shorter anterior canal, and having one 
more secondary spiral thread in each interspace. 

Eripachya ponderosa of DAILEY & POPENOE (1966) is 
early Maastrichtian in age, lacks axial sculpture, and is 
an undescribed species. 


Family MELONGENIDAE Gill, 1871 
Genus Palaeatractus Gabb, 1869 


Type species: By monotypy, Palaeatractus crassus Gabb, 1869 
from the Turonian of California. 


Diagnosis: Small, thick-shelled, pyriform, ornately sculp- 
tured melongenids with a slightly twisted columella, simple 
outer lip, and thick inner lip. 


Discussion: These are small shells, considerably smaller 
than such forms as Pyrifusus Conrad, 1858, or S'ycostoma 
Cox, 1931, with which WENz (1941) has associated Pa- 
laeatractus. The genus is, however, similar in overall shape 
to these larger forms but has stronger sculpture and a more 
bent canal than Sycostoma, and lacks the subsutural welt 
and concave band of Pyrifusus. The sculpture and shape 
of Palaeatractus recall that of the pseudolivine Pegocomptus 
Zinsmeister, 1983, and the volute Volutocorbis (Retipirula) 
crassatesta (Gabb, 1869) (ZINSMEISTER, 1977), but Pa- 
laeatractus has no pseudolivine groove on the body whorl, 
no folds on the columella, and has finer sculpture. 


Page 366 


Explanation of Figures 55 to 66 


Unless otherwise indicated, figures are x 1; specimens coated with 
ammonium chloride, except as noted. 


Figures 55-60. Palaeatractus crassus Gabb, 1869. Figure 55: 
LACMIP cat. no. 11550, from LACMIP loc. 10744, neotype, 
aperture, x3. Figure 56: LACMIP cat. no. 11552, from LAC- 
MIP loc. 10744, hypotype, section showing lack of folds on col- 
umella, x3, uncoated. Figures 57, 58: LACMIP cat. no. 11551, 
from LACMIP loc. 10744, hypotype; Figure 57, back, x3; Fig- 
ure 58, apical view, x 3. Figures 59, 60: LACMIP cat. no. 11553, 
from UCLA loc. 4214, hypotype; Figure 59, right side; Figure 
60, aperture. 


Figures 61-66. Saturnus dubius (Packard, 1922). Figure 61: 
LACMIP cat. no. 11556, from LACMIP loc. 10079, section 
showing lack of folds on columella, hypotype, uncoated. 


The Veliger, Vol. 36, No. 4 


Table 7 


Measurements (mm) of Palaeatractus crassus (Gabb, 1869). 


H D Hp Dp Ha A_ Hp 


LAGCMIP 11550 10:9* 65 7 1:9" 3'5) e232 Cor emles 
LACMIP 11551 7.8 4A 14s 256225 Ole 
LACMIP 11552 6.5 4.9 
LACMIP 11553 20.0* 19.6 2.8 56 4.7 86° 2.0 


* Specimen incomplete. Abbreviations decrypted in Introduc- 
tion. 


Palaeatractus crassus Gabb, 1869 
(Figures 55-60) 


Palaeatractus crassus GABB, 1869:148, pl. 26, fig. 26; 
COssMANN, 1901:82, text fig. 24; WENZ, 1941:1222, fig. 
3476. 


Diagnosis: Small pyriform shells with a low spire, thick 
shell, slightly twisted columella, simple outer lip, incrusted 
inner lip, and a strong, overall sculpture of squarish nodes. 


Description: Shell small, pyriform, thick; spire low; whorls 
five, rounded; suture impressed. Surface marked by prom- 
inent, straplike spiral ribbons, crossed by irregular axial 
ribs or lines; axial ribs variable in size, number, and dis- 
position, but generally of nearly even distribution, pro- 
ducing squarish nodes or tubercles at intersections with 
spiral ribbons; interspaces showing numerous fine growth 
lines. Aperture broad in middle, acute posteriorly, ex- 
tended anteriorly into moderate and slightly twisted canal; 
outer lip simple; inner lip thick, expanded roundly onto 
body whorl, extending adapically beyond aperture, with 
a well defined margin; columella without folds. 


Neotype: LACMIP cat. no. 11550. STEWART (1927) was 
unable to find Gabb’s specimens of this species. In their 


absence, a neotype is herein chosen from LACMIP loc. 
10744 (= CIT 1255). 


Hypotypes: LACMIP cat. nos. 11551-11552 from LAC- 
MIP loc. 10744 (= CIT loc. 1255), French Creek, north 
of Swede Basin; 11553 from UCLA loc. 4214, Little Cow 
Creek, Shasta Co., California. 


Dimensions: See Table 7. 


Original type locality: From the Shasta Group, from a 
canyon in the foothills, a mile (1.6 km) south of the road 
from Colusa to the Sulphur Springs near the eastern mar- 
gin of the Coast Range, Colusa County, California. 


os 

Figures 62, 63, 65: LACMIP cat. no. 11554, from LACMIP 
loc. 10079, hypotype; Figure 62, aperture; Figure 63, back; Fig- 
ure 65, right side. Figures 64, 66: LACMIP cat. no. 11555, from 
LACMIP loc. 10079, hypotype; Figure 64, aperture; Figure 66, 
back. Photographs 55, 56, 61-64 by Susuki; 57-60, 65 by De 
Leon. 


L. R. Saul & W. P. Popenoe, 1993 


Locality of the neotype: LACMIP loc. 10744, French 
Creek, north of Swede Basin, Shasta Co., California. 


Distribution: Redding Formation, Frazier Siltstone 
Member and near the base of the Melton Sandstone Mem- 
ber, Swede Creek Valley, Redding area, Shasta Co.; Great 
Valley Series, Colusa Co., California. ANDERSON (1958: 
26) listed this species from the second conglomerate above 
the base of the Pacheco Group on Bear Creek, Colusa Co., 
but the specimens have not been found at either the Cal- 
ifornia Academy of Sciences or the University of Califor- 
nia, Berkeley, Museum of Paleontology. 


Geologic age: Turonian. 


Remarks: The sculpture of squarish, flat nodes is dis- 
tinctive. Weathering causes the nodes to become pitted and 
produces a more ornate, pseudocancellate effect (Figure 
5)5)))e 

Although Gass (1869) indicated that his lot of fossils 
from south of the road from Colusa to the Sulphur Springs, 
Colusa County was from the Shasta Group, which is of 
Early Cretaceous age, this species has not been found 
associated with others of Early Cretaceous age and is pres- 
ent in beds of Turonian age in the Redding area. ANDERSON 
(1938:131) interpreted Gabb’s locality to be in the first 
range of foothills on the west side of the Sacramento Valley 
and south of the road between Colusa and Wilber Springs. 
He referred this locality to the younger “Chico” beds rath- 
er than the older “Shasta” strata. We have not seen any 
collection that might be from this vicinity, and there is no 
record of any such collection in the literature. The pos- 
sibility that a collector might stumble upon this locality 
and provide topotype or near topotype specimens cannot 
be ruled out, but the probability that the Redding area 
specimens are correctly determined is very large. The se- 
lection of this neotype provides additional characteristics 
for recognizing the genus and the species, and for classi- 
fying the genus. 

COssMANN (1901) referred three species to Palaeatractus: 
P. minimus (Hoeninghaus in Goldfuss, 1844) and P. roe- 
mert Holzapfel, 1888, from Vaals, Nederlands, “near Aix- 
la-Chapelle” = Aachen; and “Voluta” rhomboidalis Zekeli, 
1852, from Gosau, Austria. ZEKELI’s (1852) figure of “V.” 
rhomboidalis (pl. 14, fig. 9) has a more angular whorl 
profile, less twist to the anterior canal, and lacks the ex- 
panded, thickened inner lip of P. crassus. STOLICZKA’s (1867: 
120, pl. 10, fig. 21, 21a) “V.” rhomboidalis from the Ar- 
rialoor Group (Campanian-Maastrichtian) of southern 
India has a more rounded whorl profile similar to that of 
P. crassus, and may not be Zekeli’s species. The Indian 
form also does not show the expanded demarked inner lip 
of P. crassus, and Stoliczka suggested that in “V.” rhom- 
boidalis the sculpture diminishes with maturity, which is 
not true for P. crassus. None of these is a convincing Pa- 
laeatractus. 

GaABB (1869:148) gave the dimensions of his figured 
specimen as “Length .62 inch [=16 mm]; width .45 inch 
[=11.43 mm]; length of aperture .5 inch” [=12.7 mm]; but 


Page 367 


he drew a size bar (GaABB, 1869:pl. 26, fig. 26) 0.8 inch 
(=20.32 mm) long. WENZ (1941:1223, Abb. 3476) re- 
printed Gabb’s figure, which is 39 mm (=1.5 inches) high, 
and more than twice Gabb’s described height but less than 
two times his diagrammed height, as being 1/1. Three of 
the four specimens from Swede Basin in the Redding area 
are small (6.5 to 10.9 mm high) and close to the height(s) 
indicated by GaBB (1869), but one is larger (20.0 mm 
high). This specimen, although incomplete and larger than 
Gabb’s size bar, is considerably smaller than Gabb’s (or 
Wenz’) figure. Size range of the Redding specimens is 
probably representative of the species. 

The specimen from CASG loc. 1552, north end of the 
Shale Hills in Antelope Valley, Kern Co., California, iden- 
tified by ANDERSON (1958:58) as Palaeatractus crassus 1s 
not this species, but is instead a volute resembling Konistra 
biconica (ANDERSON, 1958). Although ANDERSON (1958) 
suggested that these beds were of Coniacian age, 
MATSUMOTO (1960:80) indicated that they are late Cam- 
panian-early Maastrichtian in age. 


Saturnus Saul & Popenoe, gen. nov. 


Type species: Siphonalia dubius Packard, 1922, from the Tu- 
ronian of Southern California. 


Diagnosis: Shell fusiform, spire fairly high; whorls an- 
gulately shouldered posteriorly with a moderate ramp. 
Growth lines prosocline at suture, strongly sinused at 
shoulder, and broadly arcuate across flank. Sculpture of 
spiral ribbons over riding collabral ribs; collabral ribs strong, 
rounded, accentuated by nodes at shoulder, dying out above 
and below. Aperture notched posteriorly at shoulder, si- 
phonal canal curved to left; outer lip smooth; columella 
smooth; inner lip well marked and forming a narrow pseu- 
doumbilicus at fasciole. 


Discussion: Saturnus resembles Deussenia Stephenson, 
1941, from the Late Cretaceous of the Gulf Coast, but 
lacks a subsutural collar, having only a subsutural welt. 
The posterior end of the aperture makes a broad angle 
rather than a narrow channel as in Deussenia. Although 
the notch in the growth line at the shoulder is suggestive 
of a turrid, and Saturnus bears some resemblance to Kne- 
fastia Dall, 1919, the shoulder notch of Saturnus is shallow 
and its growth line is similar to that of melongenids. 

The genus is named for the Roman god of agriculture, 
Saturnus, and is of masculine gender. 


Saturnus dubius (Packard, 1922) 
(Figures 61-66) 
Siphonalia dubia PACKARD, 1922:431, pl. 35, fig. 5. 
Diagnosus: As for the genus. 


Description: Medium-sized fusiform shells with a spire 
about one-third total shell height; pleural angle about 47°; 
protoconch unknown; suture appressed with a slight sub- 
sutural welt; body constricted posteriorly to form a shallow 


The Veliger, Vol. 36, No. 4 


Table 8 


Measurements (mm) of Saturnus dubius (Packard, 1922). 


Page 368 

H D Hp Dp 
LACMIP 11554 62.8 25.8 12.3 17.8 
LACMIP 11555 A faye 14.8 7.6 135i 
LAMCIP 11556 30.4* 20.7 — oe 


* Specimen incomplete. Abbreviations decrypted in Introduction. 


ramp, slightly swollen below nodose shoulder, and tapering 
anteriorly. Sculpture of strong, broad, rounded collabral 
ribs, about 10 per whorl, arising at shoulder and dying 
out on flank, all overridden by flat-topped spiral ribbons 
narrower than interspaces, four or five ribbons on whorl 
flanks of spire, at least 12 on body whorl flank, and about 
six on ramp. Growth lines prosocline at suture, becoming 
strongly opisthocline on ramp, sinused at shoulder, becom- 
ing orthocline over periphery and base. Aperture rather 
ear-shaped with a broad posterior notch and a stronger 
notch at shoulder; anterior canal elongate, slightly twisted, 
and inclined to the left; inner lip moderately thick, well 
demarked, rounded parietally, forming an elongate chink- 
like pseudoumbilicus along fasciole. 


Holotype: UCBMP cat. no. 12304. 


Hypotypes: LACMIP cat. no. 11554-11556 from LAC- 
MIP loc. 10079 (= CIT loc. 1164), south side Silverado 
Canyon, Santa Ana Mts., Orange Co., California. 


Type locality: “from the Chico of the Santa Ana Moun- 
tains, Orange Co., California” (Packard, 1922). 


Dimensions: See Table 8. 
Geologic age: Turonian. 


Distribution: Known from several localities, all near the 
top of the Baker Canyon Member or the base of the over- 
lying Holz Shale Member, Ladd Formation, Santa Ana 
Mountains, Orange Co., California. 


Remarks: PACKARD’s (1922:431) specimen was impre- 
cisely located, and he was unable to determine the horizon 
of this species. It resembles Deussenia ripleyana Harbison, 
1945, from the Ripley Formation of the Gulf Coast but 
is higher spired, has stronger and fewer collabral ribs, and 
a fasciole with a very narrow pseudoumbilicus. The ap- 
erture has a broader posterior notch and a stronger, wider 
shoulder notch. 


Family FASCIOLARIIDAE Gray, 1853 
Subfamily FASCIOLARIINAE Gray, 1853 


Genus Drilluta Wade, 1916 


Type species: Drilluta communis Wade, 1916, by original 
designation, from the Maastrichtian of Tennessee. 


Diagnosis: Rather slender fusiform shells with a spire 
about half total shell height. Whorls posteriorly constricted 


Ha Hs A R Dp/Hp Hp/Hs 
21.0 8.5 47° 10 1.4 1.4 
ble 4.9 44° 9 1.8 1.6 
ko est 46° aa) ne = 


to a roughened subsutural collar. Sculpture usually dom- 
inated by strong collabral transverse ribs; spiral sculpture 
well developed on basal slope, less frequently on periphery. 
Aperture notched posteriorly, siphonal canal of moderate 
length and slightly inclined to left. Inner lip callus thin; 
columella with a strong plait anterior to one or two weaker 
folds (SOHL, 1964:205). 


Discussion: WADE (1916), STEPHENSON (1941), and 
PILsBRY & OLSSON (1954) considered Drilluta to belong 
to the Volutidae, but WENZz (1943:1418) placed it in the 
Conacea. SOHL (1964:205) considers it close to Bellifusus 
Stephenson, 1941 (type species Odontofusus curvicostata 
Wade, 1926, Maastrichtian, Gulf Coast), and places it in 
the Fasciolariidae. 


Drilluta jacksonensis (Anderson, 1958) 
(Figures 67-72) 


Volutoderma? jacksonensis ANDERSON, 1958:174, pl. 21, 
fig. 1. 


Diagnosis: A large Drilluta with a weakly developed sub- 
sutural collar, moderately strong shoulder, elongate body 
whorl, 13 to 18 wide-spaced strong, sigmoidal collabral 
ribs, and faint spiral sculpture on base of body whorl and 
siphonal neck. Shoulder at about mid whorl height on 
spire. 


Description: Shell large, elongate fusiform, apical angle 
about 33°; spire broken but probably approximately of 
same length as body whorl; whorls of spire about one- 
third broader than high, with a steeply sloping, moderately 
broad and very shallowly concave ramp to noded shoulder, 
shoulder at about mid whorl height, flanks slightly convex; 
suture sinuous, appressed, with weakly developed, wrin- 
kled subsutural collar; body whorl with a steeply sloping 
concave ramp to noded shoulder, gently convex lateral 
areas, and concave gently tapering, moderately long si- 
phonal portion; axial sculpture of 13 to 18 rather widely 
spaced, collabral ribs to the whorl; ribs concave toward 
aperture, most strongly developed on shoulder of whorl, 
diminishing and disappearing rapidly anteriorly, and usu- 
ally more or less obsolete on the concave ramp; spiral 
sculpture of close-set, faint, revolving lines usually appar- 
ent only on base of body whorl and siphonal neck. Aperture 
narrow, parietal border of aperture shallowly excavated; 
columella of medium length, nearly straight, bearing prox- 


L. R. Saul & W. P. Popenoe, 1993 


Page 369 


Explanation of Figures 67 to 82 


All specimens coated with ammonium chloride; unless otherwise 
indicated figures are x1. 


Figures 67-72. Drilluta jacksonensis (Anderson, 1958). Figures 
67, 68: CAS cat. no. 445.16 from CAS loc. 445, holotype; Figure 
67, aperture; Figure 68, left side. Figure 69: LACMIP cat. no. 
11584 from LACMIP loc. 10778, hypotype, aperture. Figure 
70: LACMIP cat. no. 11562 from LACMIP loc. 10771, hypo- 
type, aperture. Figures 71, 72: LACMIP cat. no. 11557 from 
LACMIP loc. 10750, hypotype; Figure 71, aperture; Figure 72, 
back. 


Figures 73-82. Drilluta sicca sp. nov. Figure 73: CAS cat. no. 
445.31 from CAS loc. 445, holotype, aperture. Figure 74: LAC- 


MIP cat. no. 11563 from LACMIP loc. 10903, paratype, ap- 
erture. Figures 75, 79: LACMIP cat. no. 11566 from LACMIP 
loc. 10903, paratype; Figure 75, back view; Figure 79, aperture 
showing columellar folds. 


Figures 76, 80, 81: LACMIP cat. no. 11559 from LACMIP loc. 
10810, paratype; Figure 76, right side, x2; Figure 80, aperture, 
x2; Figure 81, back, x2. Figures 77, 78, 82: LACMIP cat. no. 
11565 from LACMIP loc. 10769, paratype; Figure 77, aperture; 
Figure 78, apical view; Figure 82, left side, x 1.5. Photographs 
67-70, 73-82 by De Leon; 71, 72 by Susuki. 


Page 370 


The Veliger, Vol. 36, No. 4 


Table 9 


Measurements (mm) of Drilluta jacksonensis (Anderson, 1958) and D. sicca sp. nov. 


H D Hp Dp 
D. jacksonensis 
CAS 445.16 85.0* 33.9 16.2 23.8 
LACMIP 11557 70.6* 30.0 14.4 23.0 
LACMIP 11558 32.0* 14.8t 7.6 10.8+ 
LACMIP 11562 32.0* 15.0t 7.8 10.0 
LACMIP 11584 27.8* 11.5 5.0 7.8 
D. sicca 
CAS 445.31 56.5* 26.3T 12.8 18.6 
LACMIP 11559 12.8* 6.1 1.9 4.0 
LACMIP 11560 11.4* 5.6 2.0 — 
LACMIP 11561¢ == = = == 
LACMIP 11563 70.0 22.3 11.7 16.0 
LACMIP 11564¢e bye — 8.4 = 
LACMIP 11565 34.7* 16.0 7.0 11.0 
LACMIP 11566 29:2* 14.7 ed) 13.0 
UW 91830 33 ie 13.7 6.5 10.5 


Ha Hs A R Dp/Hp Hp/Hs 
47.0* 8.7 33° 17 135) 1.9 
27.9* 7.0 35° 14 1.6 eA 
— 4.0 32°F 13 1.4 1.9 
— 4.0 40°F 14 1.3 2.0 
11.4 Poff 41° 13 1.6 1.8 
25.6 8.9 Bie 10 1.4 1.4 
6.5 ES 43° 12 Pil il3) 
= 1.2 = 11 — ile 
— — 39° 12 = 
31.0 9.0 92° 10 1.4 1.3 
— 5.5 = = 1 
12.5 4.5 41° 11 1.6 1.6 
— 4.7 38° 12 ied 1.6 
14.3 4.5 45° 12 1.6 1.4 


* Specimen incomplete; ¢ specimen crushed; @ latex pull. Abbreviations decrypted in Introduction. 


imally three oblique prominent revolving folds, anterior 
fold strongest; no basal fasciole. 


Holotype: CASG cat. no. 445.16. 


Hypotypes: LACMIP cat. nos. 11557 from LACMIP loc. 
10750 (= CIT loc. 1264); 11562 from LACMIP loc. 10771 
(= CIT loc. 1209), Salt Creek; 11584 from LACMIP loc. 
10778 (= CIT loc. 1195; UCLA loc. 4416), Stinking Creek, 
Shasta Co., California. 


Dimensions: See Table 9. 


Type locality: CASG loc. 445, Forty-nine mine, two miles 
(3.2 km) south of Phoenix, Jackson Co., Oregon. 


Distribution: Redding Formation, Bellavista Sandstone 
Member, Stinking Creek, Melton Sandstone Member, 
Little Cow Creek area, Shasta Co., California. 


Geologic age: Turonian. 


Remarks: Although ANDERSON (1958) described this spe- 
cies as lacking spiral sculpture, faint spiral lines are present 
on the base of the body whorl and siphonal neck. Drilluta 
jacksonensis differs from D. sicea in having more and nar- 
rower collabral ribs, fainter spiral sculpture, and a weaker 
shoulder that is at about mid whorl on the spire. Drilluta 
jacksonensis has a more inconspicuous subsutural collar 
than does D. sicca and than have other species of Drilluta. 
Of three similar Gulf Coast genera, Drilluta (large, col- 
lared), Paleopsephaea Wade, 1926 (type species P. mutabilis 
Wade, 1926, medium sized, not collared), and Bellifusus 
(medium sized, collared), D. jacksonensis is most like Dril- 
luta in size, shape, and columellar folds. Among Gulf Coast 
species of Drilluta, D. jacksonensis is most similar to D. 
communis (WADE, 1916:459, pl. 23, figs. 5-6; SOHL, 1964: 


205, pl. 27, figs. 12-13, 20-22) in size and shape, but has 
a wider ramp and more poorly developed subsutural collar. 


Drilluta steca Saul & Popenoe, sp. nov. 
(Figures 73-82) 


Diagnosis: A volutiform Drilluta with moderately devel- 
oped, wrinkled collar, slightly concave ramp, and 10-12 
strongly shouldered, nearly straight collabral ribs per whorl. 
On spire, shoulder at about two-thirds whorl height. 


Description: Shell medium sized, elongate volutiform; api- 
cal angle about 40°; spire shorter than body whorl; whorls 
of spire about one-third broader than high, with a sloping, 
moderately broad, and very shallowly concave ramp to 
noded shoulder; shoulder at two-thirds whorl height; flanks 
rather straight; suture sinuous, appressed with moderately 
developed, wrinkled subsutural collar; body whorl with 
concave ramp to noded shoulder, barely convex lateral 
areas, and concave, gently tapering, moderately long si- 
phonal portion. Sculpture of 10 to 12 rather widely spaced, 
nearly straight, sharp collabral ribs per whorl, over-ridden 
by spiral riblets, weak on ramp and shoulder, stronger 
abapical to the mid-flank. Aperture narrow, parietal bor- 
der of aperture shallowly excavated; columella bearing two 
oblique, moderately strong folds, anterior fold stronger, 
and a faint third, posterior fold; inner lip thin, of moderate 
width, rounded on the base of the whorl. 


Holotype: CASG cat. no. 445.31. 


Paratypes: LACMIP cat. nos. 11559-11561 from LAC- 
MIP loc. 10810 (= CIT loc. 1207), Dry Creek; 11563 
from LACMIP loc. 10771 (= CIT loc. 1209), Salt Creek; 


L. R. Saul & W. P. Popenoe, 1993 


LACMIP cat. no. 11564 from LACMIP loc. 10735 (= 
CIT loc. 1212), Little Cow Creek; LACMIP cat. no. 
11565 from LACMIP loc. 10769 (= CIT loc. 1203), Dry 
Creek, Shasta Co., California; LACMIP cat. no. 11566 
from LACMIP loc. 10903 (= CIT loc. 1622), south of 
Ashland, Jackson Co., Oregon; UW cat. no. 91830 from 
UW loc. B5900, Sidney Island, British Columbia. 


Type locality: CASG loc. 445, Forty-nine mine, two miles 
(3.2 km) south of Phoenix, Jackson Co., Oregon. 


Dimensions: See Table 9. 


Distribution: Unnamed formation, Sidney Island (coll. 
Peter Ward, 3 September 1992), British Columbia; Horn- 
brook Formation, near Phoenix, Jackson Co., Oregon; 
Redding Formation, Bellavista Sandstone Member, Fra- 
zier Siltstone Member, and Melton Sandstone Member, 
Redding area, Shasta Co., California. 


Geologic age: Turonian. 


Remarks: Drilluta sicca resembles D. distans (Conrad, 1860) 
from the Ripley Formation of the Gulf Coast, but the West 
Coast form is more strongly shouldered. Drilluta sicca is 
lower spired, has a more prominent shoulder, has fewer, 
stronger, straighter collabral ribs, and has stronger spiral 
riblets than D. jacksonensis. Drilluta sicca resembles Varens 
anae sp. nov. in overall shape, but V. anae lacks spiral 
sculpture and has a broad, straight anterior canal whereas 
that of D. sicca is slender and twisted. 

Both Drilluta sicca and D. jacksonensis are of late Tu- 
ronian age at their type locality (MATSUMOTO, 1960:77), 
but both are also found in the slightly older Bellavista 
Sandstone Member of the Redding Formation. 


Etymology: The specific name refers to the type locality 
on Dry Creek, siccus, Latin, meaning dry. 


Genus Skyles Saul & Popenoe, gen. nov. 
Type species: Skyles salsus Saul & Popenoe, sp. nov. 


Diagnosis: A medium-sized, broadly fusiform fasciolarid 
with a moderate spire and broad apical angle; suture im- 
pressed and sinuous; last whorl longer than the spire, 
roundly convex from posterior suture to neck of siphonal 
canal, constricted basally to form siphonal neck; growth 
lines and labral profile gently sigmoid, antecurrent at su- 
ture, concave aperturally below suture. Sculpture of raised 
spiral straps and low strong, nearly straight, rounded axial 
ribs, well developed on posterior half of last whorl. Ap- 
erture elliptical with a short, parallel-sided, leftward-bent 
anterior sinus; inner lip thin, oblique and twisted to the 
left siphonally, bearing one oblique inconspicuous fold at 
juncture of canal and aperture; columella twisted to left 
distally; outer lip thin, transversely lirate at its edge; si- 
phonal fasciole low, broad, enclosing a minute umbilical 
chink. 


Page 371 


94 
Explanation of Figures 83-95 


Unless otherwise indicated, figures are <1; all specimens coated 
with ammonium chloride. 

Figures 83-91. Skyles salsus sp. nov. Figures 83-86: LACMIP 
cat. no. 11568 from LACMIP loc. 10735, paratype; Figure 83, 
aperture; Figure 84, left side; Figure 85, right side; Figure 86, 
aperture. Figures 87, 90: LACMIP cat. no. 11569 from LAC- 
MIP loc. 10735, paratype; back cut away to show columellar 
fold; Figure 90, aperture. Figures 88, 89, 91: LACMIP cat. no. 
11567 from LACMIP loc. 10735, holotype; back view; Figure 
89, aperture; Figure 91, apical view, x2. 

Figures 92-94. Remera vacca sp. nov., LACMIP cat. no. 11570 
from LACMIP loc. 1446, holotype; Figure 92, back, x 3.5; Fig- 
ure 93, left side, x 3.5; Figure 94, right side. x3.5; Figure 95, 
aperture, X3.5. Photographs 83, 86, 88, 89, 95 by Susuki; 84, 
85, 87, 90-94 by De Leon. 


Discussion: Skyles is similar to Ornopsis Wade, 1926 (type 
species O. glenni Wade, 1916, Maastrichtian, Gulf Coast), 
from which Skyles differs in having the axial ribs more 
persistent posteriorly, lacking a concave subsutural band, 
having coarser, more widely spaced spiral sculpture, and 
having a shorter siphonal canal. Although the columellar 
fold of Skyles is similar to that of Ornopsis, the absence of 
a concave subsutural band in Skyles gives it a more buc- 
ciniform whorl profile. 


Page 372 


Table 10 


Measurements (mm) of Skyles salsus sp. nov. 


Dp/ 
H D Hp Dp Ha A R Hp 
LACMIP 
11567 22:42 12:0" 410) 1010935 522 12a 2e5 
LACMIP 
11568 22:0) “Al2kS= 458) “O28 Oi 1622 lien 210 
LACMIP 
11569 26.4 16.0 6.4 11.2 13.0 60° — 1.8 


* Specimen incomplete. Abbreviations decrypted in Introduc- 
tion. 


The genus is named for Scyles, a Scythian king who 
was beheaded by his brother, and is of masculine gender. 


Skyles salsus Saul & Popenoe, sp. nov. 
(Figures 83-95) 
Diagnosis: As for the genus. 


Description: Shell medium sized, broadly fusiform; spire 
about two-fifths the height of the shell, apical angle 55°; 
whorls five, evenly convex, about twice as wide as high; 
suture linear, impressed, and sinuous; last whorl about 
half as long again as spire, broadly convex from posterior 
suture to approximately beginning of siphonal canal, thence 
shallowly concave to anterior tip; growth lines and labral 
profile gently sigmoid, antecurrent at suture, concave aper- 
turally below suture. Sculpture of evenly spaced, distinct, 
raised spiral straps separated by interspaces as wide as 
spirals, numbering 13 or 14 on last whorl, and about 10 
low strong nearly straight, rounded axial ribs, well de- 
veloped on posterior half of whorl, but obsolete on siphonal 
neck. Aperture elliptical; inner lip covered with a thin 
callus wash, unevenly excavated parietally, oblique and 
gently twisted to the left in its siphonal part, bearing one 
oblique, inconspicuous, laterally compressed fold at junc- 
ture of canal and aperture; outer lip incomplete in all 
specimens at hand, but apparently thin, transversely lirate 
internally at apertural margin but smooth farther within; 
columella rather short and twisted to the left distally; si- 
phonal fasciole low, broad, rounded, smooth, enclosing 
minute umbilical chink. 


Holotype: LACMIP cat. no. 11567. 


Paratypes: LACMIP cat. nos. 11568-11569 from LAC- 
MIP loc. 10735 (= CIT loc. 1212). 


Dimensions: See Table 10. 


Type locality: LACMIP loc. 10735 (= CIT loc. 1212), 
Little Cow Creek, two miles (3.2 km) NE of Frazier 
Corners, Shasta Co., California. 


Distribution: Known only from the type locality. 


The Veliger, Vol. 36, No. 4 


Geologic age: Turonian. 


Remarks: Skyles salsus is described from three specimens. 
It resembles Ornopsis glenni Wade, 1926, the type species 
of Ornopsis, but differs in having the axial ribs persist to 
the posterior suture, lacking a concave subsutural band, 
having coarser, more widely spaced and fewer spiral ribs, 
and having a shorter siphonal canal. 


Etymology: The species is named for its type locality on 
Salt Creek, Latin, salsus, meaning salted, salty, witty. 


Subfamily FUSININAE Wrigley, 1927 
Genus Remera Stephenson, 1941 


Type species: Remera microstriata Stephenson, 1941, from 
the Maastrichtian of the Gulf Coast. 


Diagnosis: Medium-sized fusiform shells with the spire 
more than half total shell height. Whorls flat sided, or- 
namented by strong collabral ribs and subdued overriding 
spiral ribbons. Aperture lenticular, angulated posteriorly; 
siphonal canal moderately long and straight; columella 
smooth (SOHL, 1964:226). 


Discussion: Remera is represented by several species from 
the Gulf and Atlantic coastal plains Exogyra ponderosa and 
Exogyra cancellata zones. Specific differentiation within the 
genus is based, for the most part, on relatively minor dif- 
ferences in convexity of the whorl sides and sinuosity of 
the collabral ribs, and some species are based upon so little 
material that comparison is difficult. Some of these species 
may, with further study, prove to be synonyms (SOHL, 
1964:226). Remera has not been reported hitherto from 
the Pacific Coast Cretaceous nor from beds as old as the 
Turonian. 

ERICKSON (1974:207) suggests that Remera may be a 
synonym of Exilia Conrad, 1860, type species Exilia per- 
gracilis Conrad, 1860, by monotypy, Paleocene, Gulf Coast. 
STEWART (1927) indicated that Exzlia has a shallow pos- 
terior siphonal notch and placed FExilia in the Turridae, 
where most subsequent workers have left it. BENTSON (1940: 
202) was unable to find any indication of a posterior notch 
and placed it in the Fusininae, but Exzlia continues to be 
classed as a brachytomine turrid (e.g., GIVENS, 1974:91). 
The growth line of Remera has a broad posterior sinus 
like that of other Fusininae. Remera has the spire equal 
to more than half the total shell height, whereas in Exilia 
the spire is relatively shorter, and the aperture is equal to 
or longer than the spire. 


Remera vacca Saul & Popenoe, sp. nov. 
(Figures 92-95) 
Diagnosis: A small, short Remera with 15 collabral ribs. 


Description: Shell small, slender, subfusiform, with 
rounded whorls and an acute spire; apical angle about 35°; 


L. R. Saul & W. P. Popenoe, 1993 


whorls about six (spire incomplete), gently and evenly 
convex, wider than high; suture linear and impressed; last 
whorl slightly less than one-half the height of the shell, 
evenly but broadly convex, rounding abapically into a 
straight and rather short anterior canal; growth lines form- 
ing a gentle parasigmoid curve, concave on posterior part 
of body whorl, convex toward aperture anteriorly, aligned 
nearly with the shell axis. Sculpture of about 15 low, 
sinuous, round-crested collabral ribs, and numerous, fine, 
irregularly spaced, incised spiral lines; collabral sculpture 
dying out at base of body whorl, but spiral lines persisting 
to anterior end of shell. Aperture elongate-fusiform, point- 
ed posteriorly; inner lip smooth without visible columellar 
plications or callus, excavated at base of parietal wall; outer 
lip thin. 


Holotype: LACMIP cat. no. 11570. 


Type locality: LACMIP loc. 10764 (= CIT loc. 1446), 
south side Woodman Creek, Millville Quadrangle, Shasta 
Co., California. 


Dimensions: See Table 11. 


Distribution: Known only from the type locality approx- 
imately 152 m above the base of the Bellavista Sandstone 
Member of the Redding Formation. 


Geologic age: Turonian. 


Remarks: Remera vacca differs from all species previously 
assigned to this genus in being shorter. The spire does, 
however, make up more than half of the total shell height. 
This species is described from one well-preserved, nearly 
complete specimen, lacking only the apical and anterior 
sinus tips. If it is an adult, it is decidedly small for the 
genus. 


Etymology: The species is named for its type locality in 
Little Cow Creek valley, Latin, vacca, meaning cow. 


Superfamily VOLUTACEA Rafinesque, 1815 


Family VOLUTIDAE Rafinesque, 1815 


The Late Cretaceous seems to have been marked by an 
efflorescense of related large volutes in all parts of the 
world (DALL, 1907). In Dall’s view, certain morphological 
types are repeated among the species making up the volute 
group in each fauna. The disparate morphologies of each 
local group are thus more closely related than they are to 
the forms they mimic of other areas. Dall, therefore, pro- 
posed taxa and generic groupings with strong geographic 
control, but others have chosen to group the species by 
morphological similarities. Although such incompatible 
methods have resulted in a classification of Cretaceous 
volutes that needs thorough revision, such is not attempted 
in this paper. Modern volutes have been reviewed by 
WEAVER & DU PONT (1970), who followed the classifi- 
cation of PILSBRY & OLSSON (1954), which divides the 


Page 373 


Table 11 


Measurements (mm) of Remera vacca sp. nov. 


Dp/ 
H D Hp Dp Ha A _ La Hp 

LACMIP 
11570 Dh GED 1S) Aa AE SI hs wales) 


* Specimen incomplete. Abbreviations decrypted in Introduc- 
tion. 


Volutidae into 12 subfamilies. PONDER & WAREN (1988) 
combined some of the subfamilies of Pilsbry & Olsson, but 
added others and divided the Volutidae into 10 subfamilies. 
The least satisfactory of these is the Pholidotominae Coss- 
mann, 1896, queried by Ponder & Waren, in which they 
questionably submerge Volutoderminae Pilsbry & Olsson, 
1954. The four genera of Cossmann’s Pholidotominae— 
Pholidotoma Cossmann, 1896, Beisselia Holzapfel, 1889, 
Rostellites Conrad, 1855, and Gosavia Stoliczka, 1866— 
have only the posterior growth-line sinus in common. Phol- 
idotoma and Beisselia have a smooth columella and are 
probably not volutes. Cossmann’s Rostellites includes Vol- 
utoderma Gabb, 1877, Volutomorpha Gabb, 1877, and Lon- 
giconcha Stephenson, 1941, among others that PILSBRY & 
OLsson (1954) place in Volutoderminae. PILSBRY & 
OLSSON (1954:29) suggest that Gosavia may be a turrid, 
but except for its growth line, its adult shell is similar to 
that of Volutocristata Gardner & Bowles, 1934, which Pils- 
bry & Olsson have included in Atheletinae Pilsbry & Ols- 
son, 1954. Volutocristata has been shown to be a junior 
synonym of Lyrischapa Aldrich, 1911 (GIVENS, 1979), which 
is usually classed in the subfamily Fulgorarinae Pilsbry 
& Olsson, 1954. 


Subfamily VOLUTODERMINAE Pilsbry & Olsson, 1954 


The geologically oldest members of this subfamily have a 
marked posterior sinus to the growth line. The sinus is 
commonly on the shoulder in Cenomanian forms, but is 
generally broader, shallower, and closer to the suture in 
Maastrichtian forms. Sculpture may be strongly cancellate 
or Ficus-like, formed by the intersection of strong ribs and 
spirals. 


Genus Carota Stephenson, 1952 


Type species: By original designation, Carota robusta Ste- 
phenson, 1952, Cenomanian, from Woodbine Forma- 
tion, Texas. 


Diagnosis: Medium to large volutids with medium height 
spire; relatively large, strongly tilted protoconch; elongat- 
ed, gracefully curved body whorl; coarsely noded shoulder 
angle; a deep notch at intersection of shoulder angle with 
outer lip; two or three coarse folds on columella; and a 
relatively fine pattern of spiral ornamentation. 


Page 374 


Discussion: Carota, Gosavia, and Rostellaca Dall, 1907, 
have similar sculpture and growth line. Gosavia was as- 
signed by STOLICZKA (1867) to the Conidae because of its 
shape and by COssMANN (1896) and PILSBRY & OLSSON 
(1954) to the Turridae, presumably because of its growth 
line, but it has been accepted as a volute by many (e.g., 
DALL, 1907; WENz, 1943). Gosavia has five to six colu- 
mellar folds rather than the two or three of Carota. Ros- 
tellaca has three columellar folds, is shaped more like Car- 
ota, and has similar but rougher sculpture (DALL, 1907). 
Rostellaca differs mainly in having the posterior notch nearer 
the suture, a thicker, wider inner lip, and a strong twist 
to the end of the anterior siphon. 

In Carota, STEPHENSON (1952) included, in addition to 
four species from the Woodbine Formation of Texas, Volu- 
toderma? venusta Stephenson, 1936, from Banquereau 
Bank, off the east coast of Nova Scotia, and Rostellites dalli 
Stanton, 1893, from the “Pugnellus sandstone” of Turo- 
nian age, Huerfano Park, Colorado. The following two 
Pacific Slope species, Scobinella dilleri and Cordiera mi- 
traeformis, herein placed in Carota, have a posterior notch 
in the outer lip at the shoulder similar to that of Carota. 
This characteristic may prove to be an evolving trait. The 
relatively deep posterior notch distant from the suture is 
present in Cenomanian and Turonian volutes, a shallower 
notch closer to the posterior suture is common in later 
Cretaceous volutes, and most Cenozoic volutes have no 
more than a vestige of a notch against the suture. 

The pattern of the columellar folds differs on the two 
Pacific Slope species: Carota dilleri (White, 1889) has three 
nearly equal, equally spaced folds as in the type species, 
Carota robusta; but in C.? mitraeformis (Gabb, 1869) the 
two posterior folds are closer together and the two anterior 
folds are stronger. Although fold number, placing, and 
strength vary among species assigned to Carota by STE- 
PHENSON (1952), none has the same pattern as C.? mi- 
traeformis. 


The Veliger, Vol. 36, No. 4 


Carota diller: (White, 1889) 
(Figures 96-101, 106, 107) 


Scobinella dillerr WHITE, 1889:25, pl. 4, figs. 1-3; STANTON, 
1895:19. 

Volutoderma (Rostellinda) dilleri (White): DALL, 1907:10. 

““Scobinella dillert” White: STEWART, 1927:410. 

Volutoderma diller: (White): ANDERSON, 1958:175. 

Rostellinda dilleri (White): JONES, SLITER & POPENOE, 1978: 
xxii.9, pl. 1, fig. 7. 


Diagnosis: A slender, high-spired Carota with strongly 
shouldered, straight axial ribs, regular straplike spiral cords, 
and a relatively shallow growth-line notch at the shoulder. 


Description: Shell of medium size, fusiform, with about 
seven volutions; whorls of the spire angulately convex; last 
whorl elongate, shouldered posteriorly, its greatest diam- 
eter near its shoulder, concave posterior to shoulder and 
broadly convex anterior to it, tapering anteriorly to a short 
siphonal canal; growth line opisthocline on ramp, strongly 
notched at shoulder, barely convex across flank. Spiral 
sculpture of coarse, raised, revolving lines or small ridges, 
about 17 or 18 on the last whorl, broader about middle of 
whorl, narrower anteriorly and on the siphonal neck, and 
obsolete on subsutural ramp; axial ribs present on all whorls, 
strongest at shoulder, usually nine on last whorl. Aperture 
narrow, nearly parallel-sided; anterior canal narrow, 
curved, flexed gently to the left; outer lip thin, with a broad 
sinus between suture and shoulder, broadly convex be- 
tween shoulder and anterior siphon; columella with three 
strong folds of approximately equal size and spacing, 
strengthening interiorly; inner lip with pad of callus at 
posterior margin, adjacent to the anal gutter. 


Syntypes: USNM cat. no. 20123 (3 specimens). 


Hypotypes: LACMIP cat. nos. 10806 (= UCLA 59444, 
JONES et al., 1978:fig. 7), 11571-11572, 11616; all from 


Explanation of Figures 96 to 120 


Unless otherwise indicated, figures are x 1; specimens coated with 
ammonium chloride, except as noted. 


Figures 96-101, 105-107. Carota dilleri (White, 1889). Figures 
96-98, 107: LACMIP cat. no. 11571 from LACMIP loc. 10735, 
hypotype; Figure 96, aperture; Figure 97, back; Figure 98, right 
side; Figure 107, posterior growth line sinus at the shoulder, x 2. 
Figure 99: LACMIP cat. no. 11616 from LACMIP loc. 10735, 
hypotype, aperture. Figures 100, 101: LACMIP cat. no. 10806 
from LACMIP loc. 10735, hypotype; Figure 100, outer lip bro- 
ken back, showing columellar folds; Figure 101, back. Figure 
106: LACMIP cat. no. 11572 from LACMIP loc. 10735, hy- 
potype, showing columellar folds, back view, uncoated. 

Figures 102-105, 108-113: Carota? mitraeformis (Gabb, 1869). 
Figures 102-104, 113: LACMIP cat. no. 11573 from LACMIP 
loc. 10769, hypotype; Figure 102, aperture; Figure 103, back; 
Figure 104, right side; Figure 113, apical view. Figures 105, 


108: LACMIP cat. no. 11618 from LACMIP loc. 10789, hy- 
potype; Figure 105, left side; Figure 108, aperture. Figure 109: 
LACMIP cat. no. 11617 from LACMIP loc. 10789, hypotype, 
posterior growth line sinus at the shoulder, x2. Figure 110: 
LACMIP cat. no. 11574 from LACMIP loc. 10769, hypotype, 
section showing columellar folds, uncoated. Figures 111, 112: 
LACMIP cat. no. 10805 from LACMIP loc. 10789, hypotype; 
Figure 111, back; Figure 112, aperture. 


Figures 114-120. Konistra biconica (Anderson, 1958). Figures 
114-116, 120: CAS cat. no. 61935.01 from CAS loc. 61935, 
holotype; Figure 114, apical view; Figure 115, left side; Figure 
116, right side; Figure 120, aperture. Figures 117-119: LAC- 
MIP cat. no. 11619 from LACMIP loc. 10789, hypotype; Figure 
117, left side; Figure 118, aperture; Figure 119, posterior portion 
of growth line, x2. Photographs 96, 97, 100-103, 106, 110-112 
by Susuki; 98, 99, 104, 105, 107-109, 113-120 by De Leon. 


Page 375 


L. R. Saul & W. P. Popenoe, 1993 


Page 376 


The Veliger, Vol. 36, No. 4 


Table 12 
Measurements (mm) of Carvota dilleri (White, 1889) and Carota? mitraeformis (Gabb, 1869). 


H D Hp Dp 
Carota dilleri 
LACMIP 11571 49.0* 20.5 7.3 13.0 
LACMIP 11572 45.0 —_ 6.7 — 
LACMIP 11616t 49.0* 18.8 e2: 12.6 
UCLA 59444 37.8* 20.4 — — 
Carota? mitraeformis 
MCZ 21856** 17.0* O55 -— — 
LACMIP 11573 38.2 18.2 4.2 10.0 
LACMIP 11574 41.5* 27.0 — — 
LACMIP 11617 36.0* 18.0 4.7 10.0 
LACMIP 11618 46.8* 20.4 4.5 12.0 
UCLA 58445 34.0 16.4 4.9 9.4 


Ha Hs A R Dp/Hp Hp/Hs 
15.0* 3.0 49° 9 1.8 Jos3) 
— 3.3 41° — — 2.0 
13.5 3.4 Bye? 8 1.8 Zeit 
tie ae eu 8 =a i 
10.0 1.6 61° 23 2.4 2.6 
TAO Z oe 67° 19 169. 2.8 
8.0* 1.8 68° 16 Dri 185) 
10.0 2.8 oe 23 1.9 1.8 


* Specimen incomplete; f specimen crushed; ** measurements fide STEWART, 1927. Abbreviations decrypted in Introduction. 


LACMIP loc. 10735 (= CIT 1212), Little Cow Creek, 2 
miles (3.2 km) NE of Frazier Corners, Shasta Co., Cal- 
ifornia. 


Dimensions: See Table 12. 


Type locality: “Little Cow Creek valley, 18 miles (29 
km) east of Redding, Shasta Co.” (White, 1889). 


Distribution: Nanaimo Group, unnamed formation of 
Sydney Island (Canada Geol. Surv. loc. 85511 and UW 
loc. 85900), British Columbia; Hornbrook Formation, Os- 
burger Gulch Sandstone Member, Jackson Co., Oregon, 
and Siskiyou Co., California; Redding Formation, Frazier 
Siltstone Member above the horizon of Romaniceras (Yu- 
bariceras) deverioide (de Grossouvre, 1889), vicinity of Lit- 
tle Cow Creek, Shasta Co.; Gas Point Formation, Ono 
area, Shasta Co., California; Valle Formation, Upper 
Member, Cedros Island, Baja California, Mexico. 


Geologic age: Early to late Turonian. 


Remarks: DALL (1907) referred this species to Rostellinda 
Dall, 1907 (type species Volutoderma (Rostellinda) stoli- 
czkana Dall, 1907, from the Trichinopoly Group of 
Southern India), a subgenus of Volutoderma Gabb, 1877. 
However, in characterizing Rostellinda, DALL (1907:6) says 
“the sinus near the suture,” and neither he nor STOLICZKA 
(1867:87) mentions a notch at the shoulder that would 
produce a posterior emargination to the growth line similar 
to the posterior sinus of turrids. DALL (1907) based the 
type species of Rostellinda, V. (R.) stoliczkana Dall, 1907, 
upon figures of STOLICZKA (1867:pl. 7, figs. 6, 7 as Ful- 
goraria elongata d’Orbigny, 1843), and he assigned the nine 
specimens figured by STOLIZCKA (1867:pl. 7) as F. elongata 
to five new species of Rostellinda. On none of these figures 
is a posterior growth-line emargination indicated at or near 
the shoulder. Stoliczka also figured and described Gosavia 
indica Stoliczka, 1867, a species which like the type species 


of Gosavia Stoliczka, 1865, Gosavia squamosa (Zekeli, 1852), 
has a posterior notch at the shoulder and a resultant emar- 
gination of the growth line. WHITE (1889) had originally 
described Carota dillert as a Scobinella Conrad, 1848, family 
Pleurotomidae, a placement doubtless suggested by the 
posterior growth line emargination. Dall either overlooked 
this characteristic of the growth line or did not consider it 
of systematic importance in reassigning C. dilleri to Ros- 
tellinda. 

Figures of Rostellaca zitteliana (Holzapfel, 1888), type 
species of Rostellaca Dall, 1907, clearly show a posterior 
notch and emarginated growth line, but the notch and 
emargination are closer to the suture than in C. dilleri. 
DALL (1907) included four species from the Aachen chalk 
in Rostellaca which he characterized as having a “rougher 
sculpture, with nodulation of the intersections, the axial 
and spiral ridges more nearly equal in strength, the shell 
smaller, the shoulder less emphasized, and the posterior 
sinus less conspicuous.” 

Carota dilleri is similar to the type species C. robusta 
Stephenson, 1952, in overall shape and sculpture. Carota 
dillert has a slightly higher spire, more regular spiral ribs, 
and a slightly shallower posterior siphonal notch than does 
C. robusta. Carota dilleri bears a greater resemblance to C. 
robusta than it does to C. mitraeformis. Carota dilleri differs 
from C. dalli STANTON, 1893 (p. 156, pl. 33, figs. 11-13), 
which is also of Turonian age, in having higher whorls 
and fewer axial ribs. 

The growth line of Volutoderma (Rostellinda) sp. of YABE 
& NaGao, 1928 (p. 95, pl. 17, fig. 16) Cenomanian or 
Turonian, from the Mikasa Formation, Horomui area of 
Hokkaido, is not illustrated. The specimen is incomplete, 
and may not be a volute. But the growth line on Voluto- 
derma (Rostellinda) sp. of YABE & NAGAO, 1925 (p. 122, 
pl. 29, fig. 13, 13a, b) Late Cretaceous (fide HAYAMI & 
Kase, 1977:65, stage unknown), Cape Khoi beds in Al- 
exandrovsk area of north Saghalin is described as being 
sinused on the shoulder, and the illustrated growth line 


L. R. Saul & W. P. Popenoe, 1993 


(pl. 29, fig. 13b) is similar to that of C. dillert and C.? 
mitraeformis. Unfortunately although suggestive of Carota, 
the specimen of YABE & NaGao, 1925, is incomplete and 
the presence of columellar folds undetermined. 

Both STANTON (1895) and STEWART (1927) considered 
C. dilleri to be similar to Carota mitraeformis (Gabb, 1869), 
and Stewart suggested that the latter species is the im- 
mature form of “‘Scobinella” dillerx. The two species are 
distinct, even in immature individuals, and apparently had 
different substrate preferences. At Redding, C. dilleri is 
common in the sandier facies of the Frazier Siltstone, but 
C. mitraeformis is found in the Bellavista Sandstone Mem- 
ber. Carota diller: has fewer and stronger axial ribs, a 
higher and more strongly stepped spire, straighter inner 
lip, less strongly convex outer lip, stronger more equally 
developed and spaced columellar folds, a broader and more 
wrinkled whorl shoulder, and a callus pad on the posterior 
inner lip that is lacking in C. mitraeformis. 

HaGGaRT (1991:A161) reports Tragodesmoceras ashlan- 
dicum Anderson, 1902, from Hamley Point, Sydney Island, 
British Columbia, and infers an early or mid-Turonian 
age for these deposits. Carota dilleri occurs above Roman- 
iceras (Yubariceras) deverioide in the Redding area and thus 
probably ranges through most of the Turonian. 


Carota? mitraeformis (Gabb, 1869) 
(Figures 102-105, 108-113) 


Cordiera mitraeformis GABB, 1869:153, pl. 26, fig. 32. 

Volutoderma mitraeformis (Gabb): STEWART, 1927:410, pl. 
22, fig. 7; ANDERSON, 1958:174. 

Volutomorpha mitraeformis (Gabb): JONES, SLITER & 
POPENOE, 1978:xxii.9, pl. 1, fig. 6 (Volutoderma mitrae- 
formis on plate explanation). 


Diagnosis: An almost pyriform Carota with about 15 axial 
ribs on the spire; axial ribs more numerous but reduced 
in strength to that of the spiral cords on body whorl. 


Description: Shell medium sized, rather small for a volute; 
pleural angle about 65°; spire low, about 4 the total length 
of the shell, with about four or five low angulately shoul- 
dered whorls; suture slightly impressed; ramp very steep, 
narrow, with concave band just posterior to shoulder; last 
whorl rounded, pyriform, with greatest diameter of whorl 
approximately one-third distance from suture to tip of 
anterior canal, and with narrow swollen subsutural band, 
narrow concave ramp, barely noticeable shoulder, and well- 
arched flank curving convexly to anterior tip of shell; last 
whorl of mature specimens encroaching posteriorly across 
preceding whorls giving a more obtuse apical angle to shell. 
Spiral and axial sculpture nearly equal on body whorl; 
spiral cords flat-topped, numbering 16 or 17 on body whorl, 
separated by interspaces approximately equal to cords in 
width; axial sculpture strongest on spire, about 16 ribs per 
whorl, variably developed, weaker on body whorl, stron- 
gest at shoulder; ribs about equal to cords posteriorly, 
diminishing anteriorly, and usually faint or absent on an- 


Page 377 


terior half of whorl. Growth line with nearly straight trend 
perpendicular to suture but notched adjacent to suture and 
more deeply immediately posterior to shoulder at concave 
subsutural band, and having a slight retrocurrent deflec- 
tion near columellar tip. Aperture elongate, ovoid with 
well-developed posterior groove at suture, terminating pos- 
teriorly in a narrow pointed siphonal canal; outer lip thin, 
smooth within, inner lip covered by a thin wash of enamel, 
shallowly excavated on parietal wall; columella gently flexed 
to the left at its tip, columellar folds three, posterior to 
middle of aperture, anterior and middle folds stronger and 
more distant, middle and posterior folds closer; no siphonal 
fasciole. 


Holotype: MCZ cat. no. 21856. 


Hypotypes: LACMIP cat. nos. 10805 (= UCLA 58445), 
11617-11618 from LACMIP loc. 10789 (= CIT 1001), 
U.S. Highway 99, 4 miles (6.4 km) north of Redding, 
Shasta Co.; LACMIP cat. nos. 11573-11574 from LAC- 
MIP loc. 10769 (= CIT 1203), Dry Creek, Shasta Co., 
California. 


Type locality: “Colusa Co., near the Hot Springs” (GaBB, 
1869). 


Dimensions: See Table 12. 


Distribution: Redding Formation, Bellavista Sandstone 
east of Redding, Shasta Co.; Great Valley Series near the 
Hot Springs, Colusa Co., California. 


Geologic age: Early? Turonian, with Tragodesmoceras. 


Remarks: Immature specimens of this species from the 
Redding area accord exactly with the figure and descrip- 
tion of the holotype as given by STEWART (1927), and the 
Redding specimens are undoubtedly of the same species 
as the individual described by GABB (1869). Gabb reported 
this form from the “Shasta Group” (Early Cretaceous), 
but this age reference has been strongly questioned by 
STANTON (1895), STEWART (1927), and ANDERSON (1958), 
who considered the species to be of much younger age. Its 
occurrence in beds of Turonian age in the Redding area 
supports their opinion, and there is no evidence of its being 
collected from beds of Early Cretaceous age. 

STANTON (1895) considered that Carota? mitraeformis 
resembled C. dilleri (White) from the Late Cretaceous of 
Redding, and STEWART (1927) suggested that Gabb’s spe- 
cies might be an immature individual of the latter. Both 
species occur abundantly at Redding, but C. ? mitraeformis 
is more common in the Bellavista Sandstone Member, and 
C. dilleri occurs in the Frazier Siltstone Member. Carota? 
muitraeformis differs from C. dilleri in greater obliquity of 
columellar folds, which are unequally spaced and set deep- 
er within the aperture, lower spire, weaker shoulder, and 
weaker axial ribs. 

Among the forms from India illustrated by STOLICZKA 
(1867) as Fulgoraria elongata and named by DALL (1907), 
Carota? mitraeformis most resembles Rostellinda media Dall, 


Page 378 


1907 (STOLICZKA, 1867:pl. 7, figs. 4, 8, 9), but the illus- 
trations of R. media do not indicate the presence of a 
posterior sinus at the shoulder, and its spiral sculpture is 
more widely spaced. As in the case of C. dillerz, the presence 
of the sinus in C.? mitraeformis suggests that it should not 
be assigned to Rostellinda. STEWART (1927) placed C.? 
mitraeformis in Volutoderma Gabb, 1877, but that genus 
also lacks the posterior sinus at the shoulder and addi- 
tionally has considerably more widely spaced spiral sculp- 
ture. 

Carota? mitraeformis is of smaller average size (although 
if complete, LACMIP cat. no. 11574 would probably be 
more than 50 mm high) and has a much less noticeable 
shoulder than species of Carota described by Stephenson 
from the Woodbine Formation of Texas. Although some 
adult specimens of C.? muitraeformis approach Conus in 
shape, C.? muitraeformis is more commonly shaped like a 
Volutomorpha Gabb, 1877, which lacks the posterior growth 
line sinus of Carota. The sculpture of C.? muitraeformis 
resembles that of a Volutomorpha of SOHL’s (1964) group 
B and has three oblique folds on the columella, the middle 
one of which is slightly the stronger. However, whereas 
Volutomorpha group B species have from one to three folds 
that are generally not all visible in the unbroken shell, the 
three well-developed folds of C.? mitraeformis are visible, 
and the exterior of the shell shows no evidence of the total 
glaze coating that Sohl considers typical of Volutomorpha. 
All species assigned to Volutomorpha by Sohl are of geo- 
logically younger age than is C.? mitraeformis; the place- 
ment of the columellar folds and the lack of glazing and 
posterior growth line sinus may be evolving features, and 
C.? mitraeformis may be an early Volutomorpha. A more 
complete study of Cretaceous Volutidae is needed to clarify 
the generic placement of C.? mitraeformis. 


Varens Saul & Popenoe, gen. nov. 
Type species: Varens formosus Saul & Popenoe, sp. nov. 


Diagnosis: Medium sized to moderately large volutes with 
moderately high spire; having shouldered whorls, a con- 
cave ramp, and a well-developed subsutural welt or collar, 
shoulder formed by posterior ends of axial ribs; last whorl 
broadly convex about periphery, gently concave anteriorly, 
tapering gracefully to a relatively long canal. Axial sculp- 
ture of ribs, pronounced and swollen at their posterior 
ends, diminishing anteriorly on last whorl, more strongly 
developed on earlier whorls, becoming shorter and knob- 
like on more mature whorls, diminished or obsolete on last 
whorl of large adults; spiral sculpture absent; exterior 
surface apparently coated with thin glaze. Growth lines 
gently retrocurrent at suture, forming a narrow posterior 
notch against previous whorl, nearly parallel to axis over 
mid whorl, gently antecurrent on siphonal neck. Aperture 
long and moderately narrow, outer lip thin; inner lip ex- 
panded parietally, nearly straight in columellar region; 
columella flexed to the left at anterior tip, bearing near 


The Veliger, Vol. 36, No. 4 


base of previous whorl, three oblique spiral folds; folds 
progressively stronger anteriorly. 


Discussion: Rostellites gracilis STANTON (1893:157, pl. 34, 
figs. 1-3) from the “Pugnellus sandstone” of Huerfano 
Park and Poison Canyon, Colorado, may belong to this 
genus. 

No previously described volute genus shares the char- 
acteristics of three folds, the anterior strong, posterior weak, 
lack of spiral sculpture, and exterior apparently coated by 
a glaze. Volutomorpha Gabb, 1877 (type species Volutolithes 
conradi Gabb, 1860, from Maastrichtian of New Jersey) 
is exteriorly glazed but has a low to moderate spire and 
is sculptured by spiral ribs. Like Rostellana Dall, 1907 
(type species Voluta bronni Zekeli, 1852), Varens is rel- 
atively high spired, but Rostellana has the shoulder less 
well developed and lacks a glazed coating. Carota is of 
similar shape to Varens but has a growth line that is 
strongly sinused at the shoulder, lacks a glazed coating, 
and has spiral sculpture. Fulgoraria Schumacher, 1817 
(type species Voluta rupestris Gmelin, 1791, Recent from 
Japan) is of similar shape to Varens but has four to eight 
folds on the columella, apparently a larger protoconch, and 
is spirally grooved. 

Despite its scant spiral sculpture, Varens is placed in 
Volutoderminae because of its shape, number of columellar 
folds, and growth line. It resembles genera placed in Volu- 
tilithinae Pilsbry & Olsson, 1954, but has three columellar 
folds rather than the one fold of Volutilithinae. PONDER 
& WAREN (1988) combined these two subfamilies as Vo- 
lutoderminae. 

Carota? nodosa STEPHENSON, 1952 (p. 186, p1. 42, figs. 
19-21) resembles Varens in shape, but it has spiral sculp- 
ture and a strong bend to the columella at the folds, and 
Stephenson mentions no external callus wash. 

The generic name is derived from the name of a cen- 
turian in Caesar’s army, Varenus, who was noted for a 
daring act of bravery. Varens is of masculine gender. 


Varens anae Saul & Popenoe, sp. nov. 
(Figures 121-130) 


Diagnosis: A large Varens having about ten axial ribs per 
whorl on spire, with rounded flank, and obsolete sculpture 
on mature whorls. 


Description: Shell moderately large, broadly fusiform; 
apical angle about 49°; protoconch unknown; spire of five 
or six whorls, having a well-developed, narrow, subsutural 
collar, and concave ramp, expanding sharply to angulate 
shoulder; last whorl nearly smooth, broadly convex me- 
dially, gently concave anteriorly, tapering gracefully to 
nearly straight anterior siphonal canal. Growth lines gent- 
ly retrocurrent at suture forming a narrow V-shaped pos- 
terior notch, nearly parallel to axis medially, gently an- 
tecurrent on siphonal neck. Sculpture of about ten axial 
ribs, pronounced and swollen on their posterior ends, di- 


L. R. Saul & W. P. Popenoe, 1993 


Page 379 


Explanation of Figures 121 to 138 


Unless otherwise indicated, figures are x 1; specimens coated with 
ammonium chloride except as noted. 


Figures 121-130. Varens anae sp. nov. Figures 121-124: LAC- 
MIP cat. no. 11575 from LACMIP loc. 8195, holotype; Figure 
121, aperture; Figure 122, back; Figure 123, right side; Figure 
124, apical view. Figure 125: LACMIP cat. no. 11577 from 
LACMIP loc. 10886, paratype, section, showing columellar folds, 
uncoated. Figures 126-130: LACMIP cat. no. 11576 from LAC- 
MIP loc. 10886, paratype; Figure 126, aperture; Figure 127, 
back, anterior segment removed; Figure 128, back; Figure 129, 
right side; Figure 130, segment removed to show columellar folds. 


Figures 131-138. Varens formosus sp. nov. Figures 131, 132: 
LACMIP cat. no. 11579 from LACMIP loc. 10891, holotype; 
Figure 131, aperture; Figure 132, left side. Figures 133, 134: 
LACMIP eat. no. 11580 from LACMIP loc. 10891, paratype; 
Figure 133, outer lip broken back, showing folds on columella 
and long anterior siphon; Figure 134, back. Figures 135-137: 
LACMIP cat. no. 11581 from LACMIP loc. 10891, paratype; 
Figure 135, back, x2; Figure 136, aperture, x2; Figure 137, 
apical view, X2. Figure 138: LACMIP cat. no. 11583 from 
LACMIP loc. 10891, paratype, section showing columellar folds, 
uncoated. Photographs 121, 122, 125, 127, 130 by Susuki; 123, 
124, 126, 128, 129, 131-138 by De Leon. 


Page 380 The Veliger, Vol. 36, No. 4 


Table 13 


Measurements (mm) of Varens anae sp. nov. and Varens formosus sp. nov. 


H D Hp Dp Ha Hs A R Dp/Hp Hp/Hs 
Varens anae 
LACMIP 11575 62.0* 27.4 8.8 18.7 22.0* 4.4 49° 10 Dal 2.0 
LACMIP 11576 56.4* 24.0 9.6 15:3 18.7* 55) 47° 12 1.6 Ney 


LACMIP 11577 42.0* — — — — = — = = are 


Varens formosus 


LACMIP 11579 36.0* 16.0 We 10.0 WA 5.0 46° 11 1.3 3.6 
LACMIP 11578 26.2* 11.8 7.0 9.8 satel 4.5 43° 12 1.4 1.5 
LACMIP 11580 43.0* 11.8 — — — a — — — 
LACMIP 11581 16.6* 6.8 3:5 8.0* 2.3 40° 12 1.4 
LACMIP 11582 16.5* 6.4 2.0 4.6* 1.4 42° 12 DD, 


LACMIP 11583 23.8 _ — 


*Specimen incomplete. Abbreviations decrypted in Introduction. 


minishing anteriorly; ribs longer, narrower, and more 
strongly developed on earlier whorls, becoming progres- 
sively reduced, shorter and knoblike on later whorls and 
diminished on penultimate whorl and obsolete on last whorl. 
Aperture long, pinched posteriorly, expanded medially, 
contracted to the anterior siphon, outer lip thin, broadly 
and nearly evenly convex in outline; inner lip thin, parietal 
portion expanded, narrow on the columella; columella with 
three equally spaced, very oblique folds well within the 
aperture; anterior fold strongest. 


Holotype: LACMIP cat. no. 11575. 


Paratypes: LACMIP cat. no. 11558 from UCLA loc. 
2325, Silverado Canyon; LACMIP cat. nos. 11576-11577 
from LACMIP loc. 10886 (= CIT loc. 84), Santiago- 
Trabuco divide, Santa Ana Mts., Orange Co., California. 


Type locality: LACMIP loc. 8195 (= CIT loc. 82), Sil- 
verado Canyon, Santa Ana Mts., Orange Co., California. 


Dimensions: See Table 13. 


Distribution: Ladd Formation, Baker Canyon Sandstone, 
Santa Ana Mountains, Orange Co., California. 


Remarks: Varens anae differs from Varens formosus in 
having more rounded flanks especially in mature adults, 
which are considerably larger than any specimen of V. 
formosus. In specimens of V. anae and V. formosus that 
are of equivalent size, the shoulder of V. anae is less pro- 
nounced, the axial ribs are not as nodular at the shoulder, 
and the exterior seems less glazed, although this last may 
be a result of preservation. Varens anae differs from Carota 
gracilis (Stanton, 1893) of the Pugnellus sandstone, near 
Malachite and in Poison Canyon, Huerfano Park, Colo- 
rado, in being more slender. 


Etymology: The specific name refers to the occurrence of 
this species in the Santa Ana Mountains. 


Varens formosus Saul & Popenoe, sp. nov. 
(Figures 131-138) 


Diagnosis: A medium-sized, elongate, angulately shoul- 
dered Varens with about 11 axial ribs per whorl. Surface 
of shell apparently coated by glaze. 


Description: Shell medium sized, elongately volutiform; 
apical angle about 46°; spire of about five whorls, having 
narrow subsutural welt, concave ramp, and angulate 
shoulder, and nearly straight flank constricted gently about 
base to form a broad siphonal neck. Growth line obscured 
by glaze, apparently nearly parallel to axis medially, slightly 
antecurrent on siphonal neck. Sculpture of about 11 axial 
ribs, strongest at shoulder, dying out anteriorly at about 
mid whorl; no spiral sculpture; shell surface apparently 
glazed. Aperture elongate; outer lip thin; inner lip thin, 
narrow, rounded posteriorly; columellar folds very oblique, 
anterior fold strongest, posterior very weak. 


Holotype: LACMIP cat. no. 11579. 


Paratypes: LACMIP cat. nos. 11578 from LACMIP loc. 
10946, north side Silverado Canyon at the narrows; 11580- 
11583 from LACMIP loc. 10891 (= CIT loc. 1065), Ladd 
Canyon, just north of Silverado Canyon, Santa Ana Mts., 
Orange Co., California. 


Type locality: LACMIP loc. 10891 (= CIT loc. 1065), 
Ladd Canyon, Santa Ana Mts., Orange Co., California. 


Dimensions: See Table 13. 


Distribution: Ladd Formation, Baker Canyon Sandstone, 
Santa Ana Mts., Orange Co., California. 


Remarks: Specimens of Varens formosus are noteable for 
their beautifully polished appearance. Varens formosus 
resembles Carota dilleri in shape but lacks spiral sculpture 
and the posterior sinus at the shoulder. Varens formosus 


L. R. Saul & W. P. Popenoe, 1993 


resembles young V. anae in which the bulbus adult whorls 
have not been formed. Varens formosus differs from V. 
anae in being smaller and more slender, in having a stron- 
ger shoulder, a less convex body whorl, and the posterior 
columellar plait barely present. 

Carota? nodosa Stephenson, 1952, is similar in shape to 
Varens formosus, but V. formosus lacks spiral sculpture 
and has straighter axial ribs. 


Etymology: The specific name is from Latin, formosus, 
meaning beautifully formed, comely, handsome. 


Subfamily ATHLETINAE Pilsbry & Olsson, 1954 


As adults, several Athletinae have a shell that becomes 
Cassis-like or strombiform. The body whorl may have a 
rounded or angled shoulder that may be unarmed or bear 
nodes or spines. The sculpture is more or less cancellate 
in the young, becoming partly or wholly smooth in adults. 


Konistra Saul & Popenoe, gen. nov. 
Type species: Gosavia biconica ANDERSON, 1958. 


Diagnosis: A medium-sized, elongate pyriform volute with 
subsutural band, concave ramp, rounded shoulder, and 
rounded body whorl tapering to a broad anterior canal. 
Both axial and spiral sculpture present; axial sculpture 
strongest on early whorls, decreasing with maturity, and 
anteriorly over-ridden by spiral cords. Growth lines prom- 
inent, retrocurrent on subsutural band, scarcely flexed 
across flank. Aperture elliptical, outer lip thin; inner lip 
thin, expanded posteriorly; columella bearing about mid- 
way two well-developed, slightly oblique folds, flexed left 
and backward near its tip to form a well-developed anterior 
fasciole. 


Discussion: Despite the number of middle Cretaceous vo- 
lute genera already described, Konistra has a combination 
of features not found in any of them. In shape and sculpture 
Konistra resembles Carvota, Gosavia, Retipirula, Rostellaca, 
Rostellinda, Volutomorpha, and Volutoderma. Konistra is 
most similar to Gosavia but has only two columellar folds, 
whereas Gosavia has five or six columellar folds and a 
deeply sinused growth line. Konistra tends to be shorter 
spired and more round shouldered than Carota, which has 
three columellar folds and a deeply sinused growth line. 
The sculpture of Konistra is not pustulose like that of 
Retipirula, which has two oblique folds and the trace of a 
third, and an anterior end to the siphon that is not strongly 
bent back and to the left. Rostellaca and Rostellinda are 
both higher spired than Konistra and have three folds on 
the columella. Volutomorpha has an overall surface glaze, 
a growth line that is strongly sinused adjacent to the suture, 
and one prominent fold on the columella rather than the 
two of Konistra. Volutoderma has three oblique columellar 
folds and a nearly straight tip to the anterior siphon. 
The generic name is derived from Greek, Konistra, a 


Page 381 


dusty rolling place. It refers to the presence of this genus 
at Sand Flat, Shasta Co., California, and is of feminine 
gender. 


Konistra biconica (Anderson, 1958) 
(Figures 114-120) 
Gosavia biconicaANDERSON, 1958:175, pl. 75, figs. 3, 3a. 


Description: Shell medium sized; pleural angle about 66°; 
spire low, about one-fifth the total length of the shell, with 
about five or six low angulately shouldered whorls; suture 
at or covering shoulder; ramp broad and shallowly sloping; 
last whorl pyriform, with greatest diameter of whorl just 
anterior to shoulder and approximately one-fourth the dis- 
tance from suture to tip of anterior canal, with a relatively 
broad flat ramp, a subangulate shoulder, and well-arched 
flank curving convexly to constricted anterior siphonal neck; 
neck angled backward and to the left near its tip. Rough 
spiral and axial sculpture on body whorl; spiral cords 
unevenly spaced, numbering about 20 on body whorl, sep- 
arated by interspaces of somewhat variable width but ap- 
proximately equal to cord width; axial sculpture strongest 
on spire and at shoulder; ribs stronger than cords on fifth 
whorl, progressively weaker on subsequent whorls, about 
equal to cords posteriorly, diminishing anteriorly, usually 
faint or absent on anterior half of whorl, about 12 on fifth 
whorl, 10 on sixth, variably developed, weakest on body 
whorl. Growth lines prominent, with nearly straight trend 
perpendicular to suture but notched adjacent to suture and 
having a strong bend at anterior fasciole. Aperture elon- 
gate, ovoid with well-developed posterior groove at suture; 
outer lip thin, smooth within; inner lip expanded roundly 
onto body whorl, commonly encroaching above shoulder 
and exposed as a frill adjacent to suture; columella flexed 
backward and to the left near its tip; columellar folds two, 
just posterior to middle of aperture; siphonal fasciole mod- 
erately developed. 


Holotype: CASG cat. no 61935.01. 


Hypotype: LACMIP cat. no. 11619 from LACMIP loc. 
10789 (= CIT 1001), sec. 7, T32N, R4W, Redding (1946) 
quadrangle, Shasta Co., Caldifornia. 


Type locality: CASG loc. 61935 [ex CASG 1294-A], “near 
the State highway, on Sand Flat,” north of Redding, Shasta 
Co., California. 


Dimensions: See Table 14. 


Distribution: Known only from the vicinity of “Sand Flat.” 
On 1913 U.S.G.S. Redding 30’ Quadrangle, Sand Flat is 
between Buckeye and Salt creeks along U.S. highway 99, 
but is not designated on 1946 Redding 15’ Quadrangle. 


Geologic age: Turonian. 


Remarks: In overall shape and sculpture Konistra biconica 


Page 382 


The Veliger, Vol. 36, No. 4 


Table 14 


Measurements (mm) of Konistra biconica (Anderson, 1958). 


H D Hp Dp 
CAS 61935.01 43.7* 8.4 3.4 16.7 
LACMIP 11619 49.0* 21.4 5.2 5.0 


* Specimen incomplete. Abbreviations decrypted in Introduction. 


does resemble a Gosavia, but K. biconica has only two 
columellar folds rather than the five or six of Gosavia and 
lacks the growth line sinus present at the shoulder of Go- 
savia squamosa (Zekeli, 1852). Konistra biconica is super- 
ficially so similar to Carota? mitraeformis that the two are 
commonly mixed in collections, but K. biconica has one 
less fold on the columella, weaker sculpture, a nearly 
straight growth line, and a better developed anterior fas- 
ciole. 

The specimen, CASG cat. no. 1552.03, referred to Pa- 
laeatractus crassus by ANDERSON (1958:42) has two colu- 
mellar folds and resembles Konistra biconica except that 
the shoulder is well rounded and without angularity. Un- 
fortunately the anterior end is broken and the shape of the 
anterior canal unknown. Specimen CASG cat. no. 1552.03 
occurs with ammonites considered by MATSUMOTO (1960: 
80) to suggest late Campanian or early Maastrichtian age. 
The specimen is considerably larger than any other re- 
ferred to P. crassus. 


ACKNOWLEDGMENTS 


We are grateful for the loan of specimens by P. U. Rodda, 
California Academy of Sciences; D. L. Jones, U.S. Geo- 
logical Survey, Menlo Park; H. G. Richards, Academy of 
Natural Sciences of Philadelphia; D. R. Lindberg and the 
late J. H. Peck, Museum of Paleontology, University of 
California, Berkeley; the late J. A. Jeletzky, Geological 
Survey of Canada; Marilyn Kooser, University of Cali- 
fornia, Riverside; and P. D. Ward, Universtiy of Wash- 
ington, Seattle. Several elusive references were uncovered 
by Lindsey Groves, Natural History Museum of Los An- 
geles County. The paper has been critically read by N. F. 
Sohl, U.S. Geological Survey; R. L. Squires, California 
State University, Northridge; and E. C. Wilson, Natural 
History Museum of Los Angeles County. We appreciate 
their assistance in improving this paper. Photographs by 
Takeo Susuki were taken between 1958 and 1974 at the 
University of California, Los Angeles, Department of Earth 
and Space Sciences; photographs by John De Leon were 
taken in 1991 and 1992 at the Natural History Museum 
of Los Angeles County. 


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SOHL, N. F. 1967. Upper Cretaceous gastropods from the Pierre 
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SOHL, N. F. & H. A. KOLLMANN. 1985. Cretaceous actaeonellid 
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STADUM, C. J. 1973. A student guide to Orange County fossils. 
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LOCALITIES CITED 


CIT and UCLA localities have been given LACMIP num- 
bers. Most of the CIT localities of Turonian age in the 
Redding area were plotted on JONES et al. (1978:fig. 5). 
Most of the CIT localities of the northern Santa Ana 
Mountains were plotted on POPENOE (1942:fig. 2); these 
and UCLA localities were plotted on SAUL & BOTTJER 
(1982:maps 1-3). Many of the localities discussed in 
MaArTsuMOTO (1960) are also plotted therein. 

Frazier Corners was almost a mile (1.6 km) northwest 


Page 385 


of Bella Vista on the Redding (30’) quadrangle, 1901 
edition, reprinted 1913 and 1928, and also on the Shasta 
National Forest, California map of 1948. The Frazier 
Siltstone Member derives its name from Frazier Corners 
(HAGGART, 1986), and it serves as a reference point in 
several locality descriptions. However, on the Millville 
(15') quadrangle, 1953, and the Bella Vista (7.5') quad- 
rangle, 1965, Bella Vista has been moved and replaces 
Frazier Corners. 


82. CIT: = LACMIP 8195. 
84 CIT: = LACMIP 10886. 
92. CIT: = LACMIP 10100. 

445  CASG: Fossils from Forty-nine mine, 2 miles 
(3.2 km) south of Phoenix, Jackson Co., Oregon. 
Hornbrook Formation. Late Turonian. 
(MATSUMOTO, 1960:77). 

1001. CIT: = LACMIP 10789. 

1032. =CIT: = LACMIP 10726. 

1042 CIT: = LACMIP 10876. 

1065 CIT: = LACMIP 10891. 

1164 CIT: = LACMIP 10079. 

1195 CIT: (= UCLA 4416; LACMIP 10778) In bed 
of Stinking Creek, about midway between two 
north-south wire fences across creek, 2600'N, 
1100’E of SE cor. sec. 6, T32N, R3W, Redding 
(1946) Quadrangle, Shasta Co., California. Coll.: 
Popenoe and Ahlroth, 21 June 1936. Redding 
Formation, Bellavista Sandstone Member. Early 
Turonian. (MATSUMOTO, 1960:104; POPENOE et 
al., 1987:99). 

1197. CIT: (= LACMIP 10776) Block of sandstone 
crowded with Pugnellus manubriatus picked up 
from stream bed of Stinking Creek, just down- 
stream from first fence across creek upstream 
from the creek mouth, 4050’N, 44°W of SE cor. 
[2250’S, 2000’E of NW cor.] sec. 6, T32N, R3W, 
Redding (1946) Quadrangle, Shasta Co., Cali- 
fornia. Coll.: Popenoe & Ahlroth, 21 June 1936. 
Redding Formation, Bellavista Sandstone Mem- 
ber. Turonian. (JONES et al., 1978:fig.5). 

1203. CIT: (= LACMIP 10769) lens in sandstone 
cropping out in bed of Dry Creek, 700’S, 300’W 
of NE cor. sec. 6, T32N, R3W, Millville Quad- 
rangle, Shasta Co., California. Coll.: Popenoe 
and Ahlroth, 23 June 1936. Redding Formation, 
near middle of Bellavista Sandstone Member. 
Turonian. 

1207. CIT: = LACMIP 10810. 

1209. CIT: = LACMIP 10771. 

1212 CIT: (= LACMIP 10735) Little Cow Creek, 
Millville Quadrangle, Shasta Co., California. 

1255 CIT: (= LACMIP 10744) French Creek north 
of Swede Basin. 

1264 CIT: (= LACMIP 10759) Massive brown sand- 
stone cropping out in bed of small gully tributary 


Page 386 


1293D 
1346 
1438 


1446 


1552 


1622 
2209 


2325 


2360 


2757 


2759 


4214 


to Little Cow Creek, approx. 1805'S, 2250’E of 
NW cor. sec. 9, T32N, R3W, Millville Quad- 
rangle, Shasta Co., California. Coll.: W. P. Po- 
penoe, 12 April 1937. Redding Formation, base 
of Melton Sandstone Member. Turonian. 
(MATSUMOTO, 1960:105). 

CASG: = CASG 61934. 

CIT: = LACMIP 10754. 

CIT: Highest sandstone bed under lava in gully 
on N side of Little Cow Creek, about “% mile 
(0.4 km) NE of Wilsey Ranch House, near NE 
cor. SW % sec. 31, T33N, R2W, Millville Quad- 
rangle, Shasta Co., California. Coll.: W. P. Po- 
penoe, 19 March 1940. Redding Formation, Bel- 
lavista Sandstone Member. Turonian. 

CIT: (= LACMIP 10764) Near top of N slope 
of hillside SE of Alturas-Redding Hwy, S side 
Woodman Creek, 2250'S, 500'W of NE cor. sec. 
35, T33N, R3W, Millville Quadrangle, Shasta 
Co., California. Coll.: W. P. Popenoe, 23 March 
1940. Redding Formation, Bellavista Sandstone 
Member. Turonian. (POPENOE et al., 1987:99). 
CASG: South side of Antelope Valley, north end 
of Shale Hills, 500’W of center sec. 28, T26S, 
R18E, Kern Co., California. Coll.:G. D. Hanna 
and S. H. Shaw, April 1929. Panoche Forma- 
tion. Late Campanian-early Maastrichtian. 
(MATSUMOTO, 1960:80). 

CIT: = LACMIP 10903. 

UCBMP: ?Sucia Island, San Juan Co., Wash- 
ington. Cedar District Formation. Campanian. 
UCLA: Small gully entering Silverado Canyon 
from S, just W of the narrows, directly S of Holz 
Ranch house, about 1025'’N, 150’E of SW cor. 
sec. 8, T5S, R7W, El Toro Quadrangle, Santa 
Ana Mts., Orange Co., California. Coll.: W. P. 
Popenoe, 1946. Ladd Formation, top of Baker 
Canyon Sandstone. Turonian. 

CASG: “Devils Gate” on Berryessa Creek, 
12,000 feet (3700 m) below top of Chico Group 
on Hamilton Ranch, near top of big conglom- 
erate, Napa Co.?, California. Possibly Venado 
Formation. Turonian. 

USGS: Silverado Canyon, near mouth of Ladd 
Canyon, Santa Ana Mts., Orange Co., Califor- 
nia. Coll.: S. Bowers, 23 April 1903. Ladd For- 
mation, upper Baker Canyon Sandstone Mem- 
ber. Turonian. 

USGS: Near Silverado Canyon, in lower part of 
Ladd Canyon, Santa Ana Mts., Orange Co., Cal- 
ifornia. Coll.: S. Bowers, 24 April 1903. Ladd 
Formation, upper Baker Canyon Sandstone 
Member. Turonian. 

UCLA: Soft thin-bedded sandstone exposed in 
channel of Little Cow Creek, SE cor. sec. 35, 
T33N, R3W, Millville Quadrangle, Shasta Co., 
California. Coll.: W. P. Popenoe, 2 September 


4235 


4252 


5422 


7199 


7233 


7787 


7788 


8195 


The Veliger, Vol. 36, No. 4 


1959. Redding Formation, Frazier Siltstone 
Member. Turonian. 

UCLA: Dip slope of Baker Canyon Sandstone 
on Black Star Quadrangle, cropping out about 
0.3 mile (0.5 km) NW of old Holz Ranch house, 
2600'N, 700’W of SE cor. sec. 7, T5S, R7W, El 
Toro Quadrangle, Santa Ana Mts., Orange Co., 
California. Ladd Formation, Baker Canyon 
Sandstone Member. Late Turonian. 

UCLA: Banks of irrigation ditch at about 2450 
foot (750 m) elev., W of and above SP RR tracks, 
W side of Bear Creek Valley, 2.8 mile (4.5 km) 
SE of Normal School Campus at Ashland, ap- 
prox. 3100’N, 500’E of SW cor. sec. 24, T39S, 
R1E, Ashland Quadrangle, Jackson Co., Ore- 
gon. Coll.: W. P. Popenoe, 19 May 1944. Horn- 
brook Formation. Turonian. 

UCLA: Rancheria Gulch, about 1 mile (1.6 km) 
W of Henley, and approx. 400'N, 2000’W of SE 
cor. sec. 19, T47N, ROW, Yreka 30’ Quadrangle 
(1939), Siskiyou Co., California. Coll.: W. P. 
Popenoe, summer 1951. Hornbrook Formation, 
Osburger Gulch Member. Turonian. 

UCLA: between Fremont Canyon and Oak Flat 
along a south fork of Fremont Canyon at about 
1860 foot (570 m) elev., 350’N, 1050’E of SW 
cor. sec. 7, T4S, R7W, Black Star Canyon Quad- 
rangle, northern Santa Ana Mts., Orange Co., 
California. Coll.: W. P. Popenoe and J. E. 
Schoelhammer, 28 November 1952. Willams 
Formation, Pleasants Sandstone Member. Cam- 
panian. 

UCLA: Sulphur Creek, hard sandstone about 
500 feet (150 m) upstream from abandoned cabin 
on east side of creek, NE %, SW % (2500'N, 
1750’E of SW cor.) sec. 23, T32N, R5W, Red- 
ding Quadrangle (1946), Shasta Co., California. 
Coll.: P. U. Rodda, summer 1956. Redding For- 
mation, Bellavista Sandstone Member. Turoni- 
an. 

UCR: South side Silverado Canyon, elev. ap- 
prox. 1340 feet (400 m), stream drainage directly 
below UCR loc. 7785, SW %, SW % sec. 8, T5S, 
R7W, El Toro Quadrangle (1949), Santa Ana 
Mts., Orange Co., California. Coll.: Geol. 110 
class, 8 November 1975. Ladd Formation, lower 
Holz Shale. Turonian. 

UCR: South side Silverado Canyon, elev. ap- 
prox. 1370 feet (420 m), concretions in next 
stream drainage to south of UCR 7787 that leads 
to Silverado Creek, SW %, SW % sec. 8, T5S, 
R7W, El Toro Quadrangle (1949), Santa Ana 
Mts., Orange Co., California. Coll.: Geol. 110 
class, 8 November 1975. Ladd Formation, lower 
Holz Shale. Turonian. 

LACMIP: (= CIT 82) Limey sandstone bed 
near base of shale, S of roadcut at Holz Ranch 


L. R. Saul & W. P. Popenoe, 1993 


10079 


10100 


10726 


10735 


10744 


10754 


10771 


(locality may become obscured by slides), Sil- 
verado Canyon [E edge SE %4, SE % sec. 7, T5S, 
R7W, El Toro Quadrangle], Santa Ana Mts., 
Orange Co., California. Coll.: B. N. Moore, 1927. 
Ladd Formation, Holz-Baker Canyon transi- 
tion. Turonian. 

LACMIP: (= CIT 1164) S side Silverado Can- 
yon near mouth of small N-flowing gully, and 
at top of lower fossiliferous sandstone series, about 
400 feet (120 m) SE of Holz Ranch house in SE 
cor. sec. 7, T5S, R7W [1025’N, 150’E of SW 
cor. sec. 8], T5S, R7W, El Toro Quadrangle, 
Santa Ana Mts., Orange Co., California. Coll.: 
W. P. Popenoe, 15 May 1935. Ladd Formation, 
Baker Canyon Sandstone Member. Turonian. 
LACMIP: (= CIT 92) Concretions in shale 100 
feet (30 m) above stream and near fence on N 
side of Harding canyon, about “4 mile (0.4 km) 
N of road fork in Santiago Canyon at Modjeska 
Canyon junction [near section line NW %, NW 
% sec. 28, T5S, R7W, Santiago Peak Quadran- 
gle] Santa Ana Mts., Orange Co., California. 
Coll.: B. N. Moore, 1928. Ladd Formation, basal 
Holz Shale Member. Turonian. 

LACMIP: (= CIT 1032) Shale outcrop on left 
bank of Dry Creek, E of road, 1.3 mile (2 km) 
N of Frazier’s Corners, 1500’N of SE corner sec. 
5, T32N, R3W, Millville Quadrangle, Shasta 
Co., California. Coll.: W. P. Popenoe, 1933. 
Redding Formation, Frazier Silt. Turonian. 
LACMIP: (= CIT 1212) Little Cow Creek, ap- 
prox. 2 mile (3.2 km) NE of Frazier’s Corners, 
hard sandy concretions in shale, banks of gullies 
in pasture about 2500’N, 750’W of SE cor. sec. 
4, T32N, R3W, Millville Quadrangle, Shasta 
Co., California. Coll.: Popenoe and Ahlroth, 7 
July 1936. Redding Formation, Frazier Siltstone 
Member. Turonian. JONES et al. (1978:fig. 5). 
LACMIP: (= CIT 1255) W bank French Creek 
about % mile (0.8 km) N of Swede Basin, 600'N, 
600’E of SW cor. sec. 33, T33N, R2W, Millville 
Quadrangle, Shasta Co., California. Coll.: W. 
P. Popenoe, 12 April 1937. Redding Formation, 
Bellavista Sandstone Member. Turonian. 
LACMIP: (= CIT 1346) Sandstone nodules in 
shale, left bank of Little Cow Creek, about 75 
yards (70 m) NE (upstream) from intersection 
of creek bed with S line of sec. 9, and about 4% 
mile (0.4 km) downstream from Walter Melton 
farmhouse, 10 mile (16 km) NE of Redding, 
1500’N, 2200’E of SE cor. sec. 9, T32N, R3W, 
Millville Quadrangle, Shasta Co., California. 
Coll.: W. P. Popenoe and Jane Hoel, 8 July 
1937. Redding Formation, Melton Sandstone 
Member. Turonian. 

LACMIP: (= CIT 1209) Oyster bed on left bank 
Salt Creek, about % mile (0.8 km) N of gravel 


10789 


10810 


10876 


10886 


10891 


10903 


15295 


Page 387 


pits N of Alturas-Redding Hwy (U.S. 299), 
1650'S, 1200’W of NE cor. sec. 34, T33N, R3W, 
Millville Quadrangle, Shasta Co., California. 
Coll.: Popenoe and Ahlroth, 27 June 1936. 
Redding Formation, Bellavista Sandstone Mem- 
ber. Turonian. 

LACMIP: (= CIT 1001) West side of U.S. 99, 
4.0 mile (6.4 km) by road N of Hwy 99 bridge 
just N of Redding over Sacramento River, sec. 
7, T32N, R4W, Redding (1946) Quadrangle, 
Shasta Co., California. Coll.: W. P. Popenoe and 
D. W. Scharf, 15 July 1931. Redding Formation, 
Bellavista Sandstone Member. Turonian. 
LACMIP: (= CIT 1207) Right side of Dry 
Creek, at Bellavista-Sherman Rd. crossing and 
2.3 road miles (3.7 km) N of Redding-Alturas 
Hwy (U.S. 299) 2700'N, 50'W of SE cor. sec. 
31, T33N, R3W, Millville Quadrangle, Shasta 
Co., California. Coll.: Popenoe and Ahlroth, 26 
June 1936. Redding Formation, Bellavista Sand- 
stone Member. Turonian. 

LACMIP: (= CIT 1042) Limey lenses in sand- 
stone cropping out on N bank of Rancheria Gulch, 
about 1.5 mile (2.4 km) W of Henley, 210’S, 
800’E of NW cor. sec. 30, T47N, ROW, Horn- 
brook Quadrangle, Siskiyou Co., California. 
Coll.: Popenoe and Findlay, 8 September 1933. 
Hornbrook Formation, Osburger Gulch Sand- 
stone Member. Turonian. 


LACMIP: (= CIT 84) Sandstone above basal 
conglomerate. SW cor. of NE % sec. 34, T5S, 
R7W, Santiago-Trabuco divide, Santa Ana Mts., 
Orange Co., California. Coll.: B. N. Moore, 1926. 
Ladd Formation, Baker Canyon Sandstone 
Member. Turonian. 


LACMIP: (= CIT 1065) Sandstone overlying 
basal Upper K conglomerate, from crest of scarp 
on W side of Ladd Canyon, about 0.6 mile (1 
km) N of juncture of Ladd and Silverado canyons 
[1300’S, 300’E of NW cor. sec. 8, T5S, R7W, 
Black Star Canyon Quadrangle], Santa Ana Mts., 
Orange Co., California. Coll.: W. P. Popenoe, 3 
March 1933. Ladd Formation, Baker Canyon 
Sandstone Member. Turonian. 


LACMIP (= CIT 1622): Soft gray sandstones 
cropping out along irrigation ditch 150-200 feet 
(46-61 m) above and to SW of Southern Pacific 
RR tracks about 4.0 mile (6.4 km) SE of U.S. 
Hwy 99 bridge over Ashland Creek, near mid- 
point of W boundary sec. 24, T39S, R1E, Ash- 
land Quadrangle, Ashland, Jackson Co., Ore- 
gon. Coll.: W. P. Popenoe and W. A. Findley, 
12 September 1933. Hornbrook Formation, Os- 
burger Gulch Sandstone Member. Turonian. 

LACMIP: South side of Silverado Canyon near 
mouth of small N-flowing gully, about 400 feet 


Page 388 


61934 


61935 


(120 m) SE of Holz ranch house, 1025'N, 150’E 
of SW cor. sec. 8, T5S, R7W, El Toro Quad- 
rangle, Santa Ana Mts., Orange Co., California. 
Coll.: Robert Drachuk, 1979. Ladd Formation, 
top of Baker Canyon Sandstone Member. Tu- 
ronian. 

CASG: (= CASG 1293D) Near Frazier Cor- 
ners, SW %4 sec. 4, T32N R3W, Millville Quad- 
rangle, Shasta Co., California. Coll.: C. M. Cross. 
Redding Formation, Frazier Siltstone Member. 
Turonian. 

CASG: (= CASG 1294-A): 4.6 miles (7.4 km) 


66549 


85511 


The Veliger, Vol. 36, No. 4 


north of bridge at Redding, near the State high- 
way, on “Sand Flat,” Shasta Co., California. 
Coll.: F. M. Anderson. Redding Formation, Bel- 
lavista Sandstone Member. Turonian. 

CASG: Hagerdorn Ranch, 4 mile (6.4 km) NW 
of Montague, Siskiyou Co., California. Horn- 
brook Formation, probably Osburger Gulch 
Sandstone Member. Turonian. 

GSC: Hamley Point, Sydney Island, lat. 
48°36'05’N, long. 123°16'05”W, British Colum- 
bia. Coll.: J. E. Muller, 21 August 1970. Na- 
naimo Group, near base. Turonian. (POPENOE 
et al., 1987:100). 


The Veliger 36(4):389-398 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


Atlanta californiensis, a New Species of Atlantid 


Heteropod (Mollusca: Gastropoda) from the 


California Current* 


by 


ROGER R. SEAPY 


Department of Biological Science, California State University—Fullerton, 
Fullerton, California 92634, USA 


AND 


GOTTHARD RICHTER 


Forschungsinstitut Senckenberg, Senckenberganlage 25, 60325 Frankfurt a.M. 1, Germany 


Abstract. 


A new species of atlantid heteropod, Atlanta californiensis, from California Current waters 


off southern California is described on the basis of external and internal shell structure and eye, opercular, 
and radular morphologies. Although the external shell structure of A. californiensis is most similar to 
that of A. gaudichaudi, all other morphological features examined ally it most closely with A. inflata. 
The geographical distribution of A. californiensis is within the Transition Zone faunal province of the 
North Pacific Ocean. Other authors have rejected use of the radula as a taxonomic character in the 
Atlantidae. This is undoubtedly due to misinterpretation of differences within the radula that result 
from radular ontogenesis. When only the adult portion of the radula is used, interspecific differences 


are evident. 


INTRODUCTION 


In an extensive survey of the heteropod molluscan fauna 
of the California Current between about 24° and 44.5°N 
latitude, MCGowaN (1967) reported five species of atlan- 
tids. In order of decreasing abundance, they included At- 
lanta peroni Lesueur, 1817, A. lesweuri Souleyet, 1852, A. 
gaudichaudi Souleyet, 1852, A. inflata Souleyet, 1852, A. 
inclinata Souleyet, 1852, and A. turriculata d’Orbigny, 1836. 
Specimens that could not be identified as one of the above 
species were referred to Atlanta sp. (J. McGowan, personal 
communication). Along with A. peroni, Atlanta sp. was the 
most abundant atlantid and ranged over nearly the entire 
CalCOFI station grid. The species of Atlanta described 
herein is the most abundant and often the only species of 
atlantid collected from the plankton off the coast of south- 
ern California (R. Seapy, unpublished data). Thus, it is 


* Contribution 71, Ocean Studies Institute, California State 
University. 


probable that a large portion of McGowan’s Atlanta sp. is 
this previously undescribed species. Unfortunately, the 
specimens of atlantids from McGowan’s study no longer 
exist (J. McGowan, personal communication). 

Types and voucher specimens of Atlanta californiensis 
sp. nov. have been deposited in the Santa Barbara Museum 
of Natural History, Santa Barbara, California (SBMNH); 
California Academy of Sciences, San Francisco, California 
(CASIZ); National Museum of Natural History, Wash- 
ington, D.C. (USNM); and Naturmuseum und For- 
schungsinstitut Senckenberg, Frankfurt, Germany (SMF). 
Additional specimens are in the collections of A. L. Alld- 
redge (ALA) and the authors (R. R. Seapy, RRS, and G. 
Richter, GR). 


Atlanta californiensis Seapy & Richter, sp. nov. 
(Figures 1-11) 


Material examined: 134 juveniles, mature males and fe- 
males, 0.7-2.5 mm diameter; CALIFORNIA, Santa Catalina 


Page 390 


The Veliger, Vol. 36, No. 4 


Figure 1 


Atlanta californiensis sp. nov. Stereo-pair SEM photographs of holotype shell perpendicular to shell plane viewed 
from right side (2.48 mm, female; SBMNH 140126). Scale bars = a: 1.0 mm; b: 0.1 mm. 


Basin, 33°03.4’N, 118°24.7'W, 0-150 m (oblique tow); 
coll. R. R. Seapy, California State University Ocean Stud- 
ies Institute, R/V Yellowfin, 1-m plankton net (0.5-mm 
mesh), 29 August 1991, 1405-1435 hr; RRS (uncata- 
logued). 

—766 juveniles, mature males and females, 0.6-2.7 mm 
diameter; CALIFORNIA, San Pedro Basin, 33°30.2'N, 
118°25.5'W, 0-290 m (oblique tow); coll. R. R. Seapy, 
California State University Ocean Studies Institute, R/V 
Yellowfin, 3-m? plankton net (0.5-mm mesh), 13 August 
1989, 1252-1400 hr; RRS (uncatalogued). 

—126 juveniles, mature males and females, 0.6-3.2 mm 
diameter; CALIFORNIA, Santa Barbara Basin, 34°10'N, 
119°45'W, 40 m (1800-1815 hr), 30 m (1830-1845 hr) 
and 15 m (2345-2400 hr); coll. A. L. Alldredge, University 
of California, Santa Barbara, R/V Point Sur, 70-cm BON- 
GO nets (0.5-mm mesh), 4 October 1990; ALA (uncata- 
logued). 

—8 mature males, 1.2-2.5 mm diameter; NORTH PACIFIC 
OcEAN, Subarctic Boundary, 43°15’N, 165°00’W, surface 


neuston tow; coll. National Marine Fisheries Service per- 
sonnel, R/V Melville, Station 108, Manta net (0.5-mm 
mesh), 22 October 1989, 1834-1849 hr; RRS (uncata- 
logued). 

—2 juveniles and 2 mature females, 0.6—2.5 mm diameter; 
NorTH PAcIFIC OCEAN, off British Columbia, 49°35’'N, 
127°44'W, 0-250 m (oblique tows); coll. Institute of Ocean 
Sciences, Ocean Ecology, Sidney, British Columbia per- 
sonnel, Station SK-7, Cruise 9003, Series 28 (2.5-mm 
female) and Cruise 9006, Series 21 (remaining specimens), 
70-cm BONGO nets, 16 October 1990; RRS (uncata- 
logued). 


Diagnosis: A species of At/anta Lesueur with a flattened, 
transparent calcareous shell and keel. Spire of shell low 
and globular; surface smooth, with 4% whorls; whorl width 
increases rapidly in fourth whorl. Suture separating spire 
whorls shallow. Umbilicus deep and wide. Last whorl 
encircled by keel that is high and truncate along its anterior 
margin. 


R. R. Seapy & G. Richter, 1993 


Page 391 


Figure 2 


Atlanta californiensis sp. nov. a, b. Shell of holotype tilted at 50° angle. c. Apertural view of shell (1.6 mm male). 
d, e. Shell of paratype viewed from left side (2.1 mm male; SBMNH 140127). SEM photographs. Scale bars = a, 


c, d: 1.0 mm; b, e: 0.1 mm. 


Description: Shell (Figures 1-3)—Shell moderately small; 
maximal diameter 3.5 mm, with 4% whorls. Keel pene- 
trates between last and penultimate whorls in shells with 
diameter greater than about 2.0 mm (Figure 1). Keel base 
color orange-brown to red-brown. Spire low conical to 
globular in profile, lacking surface sculpture (Figure 
2a-c). Spire coloration variable; either (a) clear to uniform 
light yellow, brown, or violet, or (b) light to dark mottled 
pattern of yellow-brown to brown. Spire suture coloration 
variable, ranging from clear to light violet to purple. Um- 
bilicus wide, but narrows rapidly with penultimate whorls 
(Figure 2d, e). Inner walls of spire decalcified, whorls 
divided internally by thin, flexible chitinous membrane 
(Figure 3a). Larval metamorphosis occurs at shell diam- 
eter of 0.5-0.6 mm. 

Operculum (Figure 4)—Operculum type “c” (after RICH- 
TER, 1974); thin, transparent, oval in shape, with mono- 
gyre nucleus. Spiral portion of operculum lacks spines. 
Eyes (Figure 5a)—Eyes type “a” (after RICHTER, 1974); 


relatively small; clear, spherical lens; black pigmented base 
interrupted dorsally by triangular-shaped, unpigmented 
window. Distal portion of pigmented base lacking clear, 
transverse slit seen in type “b” eyes (Figure 5b). 

Radula (Figures 6-8)—Radula large (relative to size of 
the animal), elongate and narrowly triangular; distinct 
sexual dimorphism. In males with shell diameter of 1.7- 
1.8 mm, length of radula about 700 um, maximal width 
about 220 um, with 75-80 rows of teeth and growth angle 
about 20-22°. In largest male examined (shell partially 
destroyed and shell diameter unknown), radula length al- 
most 1000 um, maximal width 260 um, with 99 rows of 
teeth (Figure 6a). In male radula (Figure 7), central (ra- 
chidian) tooth with broad, low basal plate and relatively 
short single cusp that is always present. Lateral tooth with 
very broad, slightly curved basal plate, with one strong 
cusp at inner margin that points posteromedially. Squarish 
promontory of basal plate (characteristic of Atlantidae) 
forms a flattened hook at its posterior edge. Inner and 


The Veliger, Vol. 36, No. 4 


Page 392 


Explanation of Figures 3 and 4 


Figure 3. Shells of a, Atlanta californiensis sp. nov., and b, A. 
inflata (from tropical Atlantic). Immature specimens, frontal views. 
Transmitted light photographs. Scale bar = 0.5 mm. 


outer marginal teeth approximately same length and some- 
what shorter than corresponding lateral tooth. Marginal 
teeth long, slender, and gently curved toward tip, which 
is somewhat hooked. 

In females with shell diameter of 1.7-1.8 mm, radula 


TS 


Type a Type b 


Figure 5 


The two major eye types (“‘a” and “‘b”’) in atlantids (after SEAPY, 
1990a:fig. 2 and RICHTER, 1974:fig. 3). Key: L, lens; DP, distal 
pigment; PP, proximal pigment, UW, unpigmented window; TS, 
transverse slit. 


Figure 4. Atlanta californiensis sp. nov. “type c” operculum with 
monogyre nucleus (from 2.2 mm male). Transmitted light pho- 
tograph. Scale bar = 0.5 mm. 


700 um in length (comparable with radulae from males 
of similar size), but maximal width (160-170 um) about 
55 um less, growth angle (17-18°) about 4° less, and num- 
ber of tooth rows (60-62) about 17 fewer. The major 
difference between radulae from mature males and females 
(Figure 8a, b) is width. Some differences in tooth mor- 
phology also exist; in females, basal plates of central and 
lateral teeth narrower, but distinctly higher, and marginal 
and lateral teeth shorter than in males. 


Type material: Holotype: Shell of adult female, diameter 
2.48 mm, mounted on SEM stub (Figures la, b, 2a, b), 
SBMNH 140126. Paratypes: Shell of adult male, di- 
ameter 1.60 mm, mounted on SEM stub (Figure 2d, e), 
SBMNH 140127. Preserved and dry specimens were de- 
posited with the following museums: SBMNH 140128, 
140129; CASIZ 088117, 088118; USNM 806324; and, 
SMF 309929, 309930. 


Type locality: CALIFORNIA, Santa Catalina Basin, 
33°03.4'N, 118°24.7'W, 0-150 m. 


Etymology: The specific epithet is based on the geograph- 
ical distribution of the species, which is largely restricted 
to the California Current (see distribution below). 


Remarks: Atlanta californiensis appears to be most closely 
related to A. inflata, a very common circumtropical species. 
Like A. inflata, A. californiensis shows partial decalcifi- 


69? 


cation of the inner walls of the shell spire, type “a” eye 


R. R. Seapy & G. Richter, 1993 


a 4 b 


DB 
i 


y DIypsyyy: WD 


an 


Page 393 


Figure 6 


Complete radulae from Atlanta californiensis sp. nov. and A. inflata (from tropical Atlantic). SEM. a-c: Atlanta 
californiensis. a. Male with 99 tooth rows. b. Immature female with 56 tooth rows. c. Male with 68 tooth rows. 
d, e: A. inflata. d. Male with 98 tooth rows. e. Female with 80 tooth rows. a, b: SEM; c-e: transmitted light. Scale 


bars = a, b: 0.1 mm; c-e: 0.1 mm. 


6699 


morphology, type “c” opercular morphology, sexual di- 
morphism of the radula, and similarities in the shape of 
the radular teeth and radular morphogenesis. The radulae 
of the two species differ, however, in that the radulae from 
both male and female A. californiensis (Figure 6a-c) are 
distinctly broader and consist of fewer tooth rows than the 
radulae of A. inflata (Figure 6d, e). The largest A. cali- 
forniensis radula examined (Figure 6a) was from a large 
adult male and measured 1000 um in length, with 99 rows 
of teeth. In contrast, the radula of the largest adult A. 
inflata examined by RICHTER (1987) was 590 um in length, 
with 113 tooth rows. Although the radulae of both species 
are sexually dimorphic, the intersexual differences are 
greater in A. californiensis. 

While the body and internal shell morphology of Atlanta 
californiensis are most similar to those of A. inflata, the 
external shell morphologies of the two species are quite 
different. The shell spire consists of about 3% whorls in 
A. californiensis and about 4% whorls in A. inflata (Figure 
9a, b). The result of this difference is that the shell diameter 
of a specimen of A. californiensis at four whorls would 
be more than twice that of A. inflata at four whorls (Figure 
10). The whorls of A. californiensis are more inflated and 
grow faster than those of A. inflata. These differences are 


seen clearly by viewing the shells along the shell axis using 
transmitted light (Figure 3). The lack of sculpture on the 
spire whorls of A. californiensis contrasts with the raised 
spiral ridges on the spire of most A. inflata (Figure 10). 
This is a variable feature in A. znflata, however, since these 
ridges can be weakly expressed or even lacking (TESCH, 
1909; RICHTER, 1987). Lastly, the umbilicus is wide in A. 
californiensis (Figure 2d, e) and narrow in A. inflata 
(RICHTER, 1987:figs. 9-12). 

The external shell morphology of Atlanta californiensis 
is most similar to those of A. gaudichaudi and A. peroni. 
The three species have several features in common: (1) the 
shells have low spires that consist (Figure 9) of about 3% 
to 3% whorls, (2) the shell surfaces are smooth and lack 
surface sculpture, and (3) the sutures between the first and 
second whorls are shallow, while those between subsequent 
whorls are deeply incised (for A. californiensis see Figure 
1b; for A. peroni see SEAPY, 1990a:fig. 4g, h; for A. gau- 
dichaudi see NEWMAN, 1990:fig. 2b, c). Suture pigmen- 
tation in A. californiensis ranges from clear (similar to A. 
peronz) to light violet to purple (similar to A. gaudichaudz). 


Distribution: Members of the family Atlantidae (Proso- 
branchia: Gastropoda) are predominantly tropical to sub- 


Page 394 The Veliger, Vol. 36, No. 4 


Explanation of Figures 7 and 8 


Figure 7. Atlanta californiensis sp. nov. Portion of radula from indicate row 60 on each radula. c, d. Morphogenesis of male 

mature male, including (from left to right) central (rachidian), radula at cross-rows 10-14 and 69-80, respectively. Photographs 

lateral, and marginal teeth. SEM. Scale bar = 50 um. from different radulae. SEM. Scale bars = a, b, d: 50 um; c: 10 
um. 


Figure 8. Atlanta californiensis sp. nov. a, b. Portions of radulae 
from mature male and female specimens, respectively. Arrows 


R. R. Seapy & G. Richter, 1993 


Page 395 


Figure 9 


Sketches of shell spires from three species of Atlanta viewed from right side of shell. a. A. californiensis sp. nov. b. 
A. inflata. c. A. gaudichaudi. Sketches b and c after SEAPY (1990a:fig. 6). Scale bar = 0.5 mm. 


tropical in distribution (THIRIOT-QUIEVREUX, 1973). Most 
of the specimens of Atlanta californiensis collected to date, 
however, have come from temperate waters of the Cali- 
fornia Current off the coast of southern California. The 
California Current is a broad, sluggish and cold current 
that warms gradually as it flows southward off the Pacific 
coast of North America. Tropical to subtropical species of 
atlantids are encountered commonly only in the southern 
portion of the California Current, south of about 34°N 
(McGowan, 1967). 

Biogeographically, the California Current comprises the 
southeastern portion of the Transition Zone faunal prov- 


ince (Figure 11). This faunal province corresponds to the 
Transitional Domain of DODIMEAD et al. (1963), and ex- 
tends southeastward in the California Current, north- 
eastward in the Alaskan Current (to about 50°N) and 
westward across the North Pacific Ocean to Asia in a 
narrow (1-2° latitude) band located to the north of the 
Subarctic Boundary at about 40-41°N. The Transition 
Zone faunal province is bounded (Figure 11) by the Sub- 
arctic Pacific faunal province to the north, the Central 
North Pacific faunal province to the south, and the North 
American Continent to the east (FAGER & McGowan, 
1963; McGowan, 1986). 


Figure 10 


Shells of a, Atlanta californiensis sp. nov., and b, A. inflata (from tropical Atlantic). Lines between triangular marks 
indicate shell diameter at four whorls. SEM. Scale bar = 1.0 mm. 


Page 396 


The Veliger, Vol. 36, No. 4 


CENTRAL NORTH 
PACIFIC 


Figure 11 


Biogeographical faunal provinces (Subarctic Pacific, Transition Zone and Central North Pacific) in the eastern 
North Pacific Ocean. Solid line denotes the Subarctic Boundary (after DODIMEAD e¢ al., 1963). Northern limits of 
Transition Zone indicated by dashed line (based on DODIMEAD et al. (1963:fig. 216). Southern limits of the Transition 
Zone defined by Subarctic Boundary and its southeasterly extension to Baja California (shown by dashed line; 
based on euphausid distribution patterns in BRINTON, 1962). Collection records for Atlanta californiensis sp. nov.: 
large solid circles = southern California (San Pedro, Santa Catalina, and Santa Barbara basins); large open circle 
= oceanic waters off British Columbia; solid triangle = oceanic waters north of Subarctic Boundary. Open triangle 
= report of KOZLOFF (1987) for ‘“‘A. gaudichaudi”’ from oceanic waters off Washingion. Small open circles = records 
of McGowan (1967) for Atlanta sp. from the California Current region off Pacific coast of North America. 


Specimens of Atlanta californiensis have been identified 
by RRS from Transition Zone waters to the north of the 
Subarctic Boundary, oceanic waters off British Columbia, 
and three areas off southern California—San Pedro Basin, 
Santa Catalina Basin and Santa Barbara Basin (Figure 
11). KOZLOFF (1987:208) reported that A. gaudichaudi “may 
be expected in oceanic plankton” off Washington. How- 
ever, he qualified the identification by stating that it was 
“perhaps a form of A. peroni,” although this remark could 
be based on a similar statement about A. gaudichaudi made 
by TEscH (1949:17). Because A. gaudichaudi was not re- 
corded by MCGOwAN (1967) from California Current wa- 


ters north of about 33°N and the shell of A. californiensis 
is most similar to this species (see above), we are reasonably 
certain that the species identified by KOZLOFF (1987) as 
A. gaudichaudi is actually A. californiensis. 

The records of McGowan (1967) for Atlanta sp. are 
included in Figure 11 because we consider that a large 
proportion of the specimens (certainly those collected north 
of about 34°N) that were relegated by McGowan to Atlanta 
sp. were A. californiensis. Our reasoning for this conclu- 
sion follows. Among the atlantids reported by MCGOWAN 
(1967) from the California Current, the only species that 
ranged to the north of 34°N were Allanta sp. and A. peront. 


R. R. Seapy & G. Richter, 1993 


It is conceivable that McGowan misidentified A. califor- 
niensis as A. peroni under certain conditions (shells clear, 
spire and suture pigmentation absent), since the general 
shell morphologies of the two species are similar in that 
the spires consist of about 3% whorls and lack sculpture 
(discussed above). It is probable, however, that McGowan 
identified most A. californiensis as Atlanta sp., since most 
A. californiensis can be distinguished from A. peroni on 
the basis of spire coloration (normally clear, but occasion- 
ally light pink in A. peroni [SEAPY, 1990a]; yellow, brown, 
or violet, often with a mottled pattern in A. californiensis) 
and keel base coloration (clear, becoming golden-brown in 
A. peroni [SEAPY, 1990a]; orange-brown to red-brown in 
A. californiensis). 

Based on the collection records in Figure 11, Atlanta 
califormiensis is clearly a Transition Zone species. We are 
not aware of any records for A. californiensis from Sub- 
arctic Pacific or Central North Pacific waters. No collec- 
tion records for any species of atlantids exist to our knowl- 
edge from Subarctic Pacific waters, and extensive collections 
of atlantids from Hawaiian waters (SEAPY, 1990a) have 
never recorded A. californiensis. A Transition Zone dis- 
tribution has been characterized previously for only one 
other species of heteropod, Carinaria japonica (SEAPY, 1974). 

The vertical distribution of Atlanta califormensis has 
not been resolved in detail. However, based on samples 
collected with opening-closing BONGO nets in San Pedro 
Basin (Seapy, unpublished data), the daytime vertical range 
appears to be largely limited to the epipelagic zone (surface 
to about 150 m off southern California). Opening-closing 
net samples have not been collected at night, and the ques- 
tion of whether or not nocturnal vertical migration takes 
place in this species remains to be determined. However, 
we suspect that upward nocturnal migration does occur 
since vertical migration was reported (SEAPY, 1990b) for 
other species of atlantids whose ranges also extended into 
the lower portion of the epipelagic zone off Hawaii. 

An interesting aspect of the vertical distribution of Af- 
lanta californiensis is that large numbers of individuals 
have been collected in surface samples taken with neuston 
nets on a number of occasions in San Pedro Basin (Seapy, 
unpublished data). The animals in these samples were 
exclusively males. Similar observations of high densities 
of male heteropods in the neuston were made by Richter 
(unpublished data) for three species—Protatlanta souleyeti 
(Smith, 1888), A. oligogyra Tesch, 1908, and Firoloida des- 
maresti Lesueur, 1817—during Cruise 51 of the R/V Me- 
teor in the central, tropical Atlantic Ocean during 1979. 
Heteropods are relatively uncommon in the neuston, but 
we have found that when they occur in high abundances 
most (if not all) of the individuals are mature males. These 
males do not appear to assemble in the uppermost water 
layer for feeding purposes, since their guts are usually 
empty (Richter, unpublished data). Perhaps this behavior 
is similar to that seen in mosquitoes, black flies, and other 
dipterans that exhibit aerial mating (reviewed by DOWNEs, 
1969). Males assemble in large swarms and individual 
females enter the swarm briefly to be captured by a male, 


Page 397 


drop out of the swarm, and mate. This behavior functions 
to bring the sexes together from dispersed populations. 


Discussion: The radula as a taxonomic character—The util- 
ity of the radula as a taxonomic character in the Atlantidae 
has been questioned and rejected by a number of workers 
(see below). We suggest that this rejection has resulted 
from a lack of understanding of radular ontogenesis. Since 
the teeth that are produced first are not cast off from the 
anterior end of the radula as they outwear their use, all 
growth stages of the radula are present in mature animals. 
As a consequence, the number of tooth rows increases 
continuously as the animal grows. 

Because the shapes of the radular teeth change dra- 
matically during ontogenesis, the radular characterizations 
given above apply exclusively to the mature portions of 
adult radulae. In most gastropods, morphogenesis of the 
radular teeth during ontogeny is restricted to the first few 
rows of teeth in the larval and post-larval animals (STERKI, 
1893). In the Atlantidae, however, the transformation of 
tooth shapes continues for the greater part of radular growth 
(RICHTER, 1961, 1963). 

The following characterization of morphogenetic changes 
in the radular teeth of Atlanta californiensis are applicable 
in principal to other atlantids. The teeth that are initially 
produced in the larva include a central rachidian tooth 
with a more-or-less square basal plate and a long, strong 
cusp. The corresponding lateral teeth are short and bi-, 
tri-, or even polycuspid. There is only one short marginal 
tooth on either side of the lateral teeth. In about rows 7 
to 10 the second (outer) marginal teeth appear and the 
radula by now shows the regular taenioglossate tooth for- 
mula of M,M,LRLM,M, (Figure 8c). At this stage of 
radular growth, there are no differences between males 
and females. The lateral teeth are strongly bicuspid and 
a rudimentary third cusp is present, but the third cusp 
disappears completely in the next few rows. The second 
(outer) cusp of the lateral teeth gradually decreases in size 
to an accessory denticle and then disappears altogether by 
about rows 50 to 60, generally later in females than in 
males. However, in males the teeth continue to change and 
attain their final shape after an additional 10 to 20 rows 
(Figure 8d). 

From the above description of radular morphogenesis, 
it is clear that only the adult portion of the radula should 
be used as a taxonomic tool and that radular morphology 
is nearly useless when applied to juvenile specimens. Ear- 
lier workers presumably did not appreciate the complex- 
ities of radular morphogenesis, which would explain why 
a number of them (e.g., BUCHMANN, 1924; TESCH, 1949; 
VAN DER SPOEL, 1976) concluded that the radula is of no 
taxonomic importance in the Atlantidae. 


ACKNOWLEDGMENTS 


The specimens used in this study were largely collected 
from southern California waters by plankton and neuston 
nets deployed from the R/V Yellowfin of the Ocean Studies 
Institute, California State University. We are grateful to 


Page 398 


Captain J. Cvitanovich and the crew of the Yellowfin for 
their help. A. L. Alldredge, University of California, Santa 
Barbara, provided a series of plankton samples from the 
1990 “Spirit” cruise in Santa Barbara Basin. D. L. Mack- 
as, Institute of Ocean Sciences, British Columbia, for- 
warded a series of plankton samples from the Institute’s 
zooplankton archives. K. Bigelow, National Marine Fish- 
eries Service, Honolulu, Hawaii Laboratory, observed at- 
lantids in a plankton sample collected from Subarctic 
Boundary waters and forwarded the specimens to RRS. 
The manuscript has been greatly improved by the reviews 
of several early drafts by F. G. Hochberg, Jr., Santa Bar- 
bara Museum of Natural History, Santa Barbara, Cali- 
fornia. We thank S. Karl for SEM operation, photography, 
and printing of Figures 1 and 2. 


LITERATURE CITED 


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BUCHMANN, W. 1924. Uber den Pharynx der Heteropoden. 
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DopIMEaD, A. J., F. FAVORITE & T. HiRANO. 1963. Salmon 
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DownEs, J. A. 1969. The swarming and mating flight of Dip- 
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Facer, E. W. & J. A. McGowan. 1963. Zooplankton species 
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Koz.orF, E. N. 1987. Marine invertebrates of the Pacific 
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McGowan, J. A. 1967. Distributional atlas of pelagic molluscs 
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McGowan, J. A. 1986. The biogeography of pelagic ecosys- 
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Netherlands 29 May-5 June 1985. UNESCO Technical 
Papers in Marine Science, Number 49. 

NeEwMaN, L. J. 1990. The taxonomy, distribution and biology 
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opoda) from the Great Barrier Reef, Australia. American 
Malacological Bulletin 8:85-94. 

RICHTER, G. 1961. Die Radula der Atlantiden (Heteropoda, 
Prosobranchia) und ihre Bedeutung ftir die Systematik und 
Evolution der Familie. Zeitschrift fur Morphologie und 
Okologie der Tiere 50:163-238. 

RICHTER, G. 1963. Untersuchungen zur Morphogenese der 
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sionsverlag), Veroffentlichungen des Instituts fur Meeres- 
forschung in Bremerhaven. Drittes meeresbiologisches Sym- 
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RICHTER, G. 1974. Die Heteropoden der ‘““Meteor”-Expedition 
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RICHTER, G. 1987. Zur Kenntnis der Gattung Atlanta (III). 
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(Prosobranchia: Heteropoda). Archiv fir Molluskenkunde 
117:177-201. 

SeaPy, R. R. 1974. Distribution and abundance of the epi- 
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The Veliger 36(4):399-404 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


The Gastropod Terebra santana Loel & Corey, 1932, 


from the Lower Miocene Vaqueros Formation, 


Southern California, Belongs in the 


Cerithiid Genus Clavocerithium s.s. 


RICHARD L. SQUIRES 


Department of Geological Sciences, California State University, 
Northridge, California 91330, USA 


Abstract. Re-examination of the primary type material and numerous other specimens of the gas- 
tropod Terebra santana Loel & Corey, 1932, which is locally very abundant in the lower Miocene 
Vaqueros Formation of California, reveals that the species is a certhiid belonging to the genus Clavo- 
certhium sensu stricto. This is the first report of Clavocerithium s.s. in the New World and its first record 
in rocks younger than Eocene. Clavocerthium (Clavocerithium) santanum is reported for the first time 
from the Vaqueros Formation in the upper Sespe Creek area, Ventura County, southern California. 


INTRODUCTION 


LOEL & Corey (1932), in their monographic study of the 
lower Miocene Vaqueros Formation in California, named 
and briefly described the gastropod Jerebra (Subgenus = 
?) santana LOEL & CoREY (1932:236-237, pl. 47, figs. 8a, 
8b, 9, 10, 11). They reported that this Vaqueros Formation 
species is very abundant wherever present. SCHOELLHA- 
MER et al. (1981), BLUNDELL (1983) and DANIEL (1989) 
also reported very abundant specimens of this gastropod 
from various outcrops in the southern California area. 
These reports of such great abundance of a Terebra sug- 
gested that it had been misidentified as to genus, because 
modern Jerebra is a predatory gastropod and makes up a 
small part of the populations of modern molluscan com- 
munities; one would expect it to be similarly uncommon 
in the fossil record. John G. Vedder and Wendell P. 
Woodring in SCHOELLHAMER et al. (1981) put the genus 
name in quotation marks when referring to “7erebra” 
santana because they had reservations about using this 
genus name. 

The purpose of this report is to show that Loel & Corey’s 
Terebra santana is a cerithiid and not a terebrid. Exami- 
nation of the holotype and three paratypes of 7. santana, 
as well as numerous other specimens from southern Cal- 
ifornia, revealed that this species belongs to the cerithiid 
genus Clavocerithium Cossmann, 1920. 


The locally great abundance of Loel & Corey’s species 
fits in well with what is known about cerithiids. Modern 
species are very abundant in places like tidal flats. For 
example, I have observed scattered, densely packed patches 
of Certhium stercusmuscarum Valenciennes, 1832, on the 
tidal sandflat at San Felipe, Baja California, Mexico. 
Brusca (1980) and SCHMIDT (1987) reported that this 
species is extremely common on tidal flats in the northern 
Gulf of California, and specimens aggregate in gigantic 
clumps wherever a semihard sandy substrate is available. 
The specimens of Clavocerithium (C.) santanum (Loel & 
Corey) in the Vaqueros Formation are always in the near- 
shore-marine lower part of the formation, where there is 
gradation with the coastal-plain deposits of the underlying 
Sespe Formation. The specimens of C. (C.) santanum in 
the lower Vaqueros Formation are probably associated 
with tidal flats and nearshore storm-related lag deposits 
that developed in this zone of gradational nonmarine and 
marine environments. One of the paratypes of this species 
was reported by LOEL & Corey (1932:79) as possibly 
coming from an estuarine deposit. 

Abbreviations used for catalog and/or localities are: 
CSUN, California State University, Northridge; LAC- 
MIP, Natural History Museum of Los Angeles County, 
Invertebrate Paleontology Section, UCMP, University of 
California Museum of Paleontology (Berkeley). Localities 
cited in this report are described under “Localities Cited.” 


Page 400 


CALIFORNIA 


NEVADA 


San Francisco 


Figure 1 


Geographic distribution of Clavocerithium (C.) santanum (Loel & 
Corey, 1932). Localities are numbered from south to north. (1) 
Santa Ana Mountains, Orange County; (2) San Joaquin Hills, 
Orange County; (3) Big Mountain, north side of Simi Valley, 
Ventura County; (4) Oak Ridge area, Ventura County; (5) Upper 
Sespe Creek, Ventura County; (6) Near Buellton, Santa Barbara 
County; (7) Eagle Rest Peak area, Kern County; (8) Junipero 
Serra Peak region, Monterey County. Question mark (‘‘?”) de- 
notes tentative identification by LOEL & Corey (1932). The 
upper Sespe Creek area (No. 5) is a new report for this species. 


COMMENTS ON GEOGRAPHIC 
DISTRIBUTION 


LoEL & Corey (1932) reported that this species, Clavo- 
cerithium (C.) santanum, ranged from Orange County to 
Santa Barbara County, southern California. They also 
reported that the species may be present in central Cali- 
fornia, as far north as Monterey County (Figure 1). The 
type locality (locality UCMP 6128) is in Arroyo Trabuco 
in the southern part of Plano Trabuco, southern Santa 
Ana Mountains, Orange County. The exact location of 
this UCMP 6128 is not known, but I visited the general 
area and found specimens of C. (C.) santanum in greenish- 
gray to reddish-gray exposures of very fine-grained sand- 
stone that apparently are in the zone of intergradation 
between the lower part of the Vaqueros Formation and 
the upper part of the Sespe Formation. 

Other workers (SCHOELLHAMER et al., 1981; DANIEL, 


The Veliger, Vol. 36, No. 4 


Figure 2 


A hand specimen (hypotype LACMIP 12102) showing the dense 
packing of Clavocerithium (C.) santanum (Loel & Corey, 1932) 
at locality CSUN 1185, Hicks Canyon, northern Santa Ana 
Mountains, Orange County, southern California. Magnification 
is X1.1. 


1989) have confirmed the presence of Clavocerithium (C.) 
santanum in the Santa Ana Mountains. DANIEL (1989) 
found several beds in Hicks Canyon in the Santa Ana 
Mountains, where specimens constitute as much as 50% 
of the rock. I visited this area and also found scattered, 
densely packed concentrations at locality CSUN 1185 
(Figure 2). 

BLUNDELL (1983) reported this species from several lo- 
calities in the Big Mountain area, north side of Simi Val- 
ley, southern California. His specimens are stored in the 
CSUN collection. Only at locality GSUN 555 are the 
specimens sufficiently well preserved to be identified as 
Clavocerithium (C.) santanum. All of the specimens that 
Blundell collected from other localities in the area are 
poorly preserved and could only be identified as certhi- 
aceans. LOEL & Corey (1932) did not report their species 
from the Big Mountain area. 

REID (1978) and SQUIRES & FRITSCHE (1978) reported 
abundant specimens of the potamidid gastropod Potamides 
sespeenis Loel & Corey, 1932, from numerous CSUN lo- 
calities in the Vaqueros Formation, upper Sespe Creek 
area, Ventura County, southern California, but upon re- 
examination the specimens from CSUN 428 proved to be 
Clavocerithium (C.) santanum. This is the first documented 
report of this species from this area. At most of the other 
localities, specimens are poorly preserved and could only 
be identified as certhiacean. Potamides sespeensis, with its 
distinctive noded ornamentation and spiral ribbing, was 
collected from localities CSUN 159 and 401. BADGER (1957) 
tentatively reported this species from the Sespe Creek area. 
His collections are now stored at LACMIP; the specimens 
are poorly preserved but appear to be C. (C.) santanum. 


R. L. Squires, 1993 


SYSTEMATIC PALEONTOLOGY 
Family CERITHIIDAE Fleming, 1822 
Subfamily CERITHIINAE Fleming, 1822 
Genus Clavocerithium s.s. Cossmann, 1920 


Type species: By original designation Cerithium lacazei 
“Vasseur” Cossmann, 1897, 1898, upper? Eocene of the 
Lower Loire River area, Brittany, northwestern France. 
See Housrick (1978) for a discussion of the authorship 
of this species. 


Clavocerithium (Clavocerithium) santanum 


(Loel & Corey, 1932) 
(Figures 3-12) 


Terebra (Subgenus = ?) santana LOEL & Corey, 1932:236- 
237, pl. 47, figs. 8a, 8b, 9, 10, 11). 

Terebra santana Loel & Corey, 1932: KEEN & BENTSON, 
1944:200. 


Supplementary description: Shell small in size (up to 
26.5 mm height), elongate, high-spired, approximately 11 
whorls, solid. Suture distinct, slightly channeled. Proto- 
conch low, conical? shape. Upper spire whorls straight 
sided to slightly convex for the first 3 to 15 mm in height 
(usually just the first 6 mm), grading into tabulate whorls, 
lower spire whorls and body whorl prominently tabulate, 
rarely convex; each whorl taller than the previous whorl. 
Upper and middle spire whorls with 4 to 5 moderately 
heavy, equidistant spiral ribs (rarely preseved), anterior- 
most spiral rib situated in sutural area. Penultimate and 
body whorls smooth. Aperture oblique, small, approxi- 
mately % to % of shell length. Columella concave with 
central oblique plait that coincides in position with colu- 
mellar side of anterior canal; thin to moderately thick 
columellar callus detached along outer side. Outer lip sin- 
ous, and growth lines on body whorl sinuous. Anterior 
canal short but distinct, slightly reflexed backward. 


Type material and type locality: Holotype, UCMP 31608 
and paratypes, UCMP 31609 and 31610, all three from 
locality UCM P 6128, Trabuco Canyon, Santa Ana Moun- 
tains, Orange County, southern California; paratype, 
UCMP 31611, locality UCMP A-253, Wiley Canyon, 
Oak Ridge area, Ventura County, southern California. 


Geologic range: Early Miocene. 


Distribution: Vaqueros Formation, southern California, 
and tentatively central California: Santa Ana Mountains, 
Orange County (LOEL & Corey, 1932; SCHOELLHAMER 
et al., 1981; DANIEL, 1989); San Joaquin Hills, Orange 
County (LOEL & Corey, 1932); Wiley Canyon in Oak 
Ridge area and near mouth of Grimes Canyon, eastern 
Ventura County (LOEL & Corey, 1932); Big Mountain, 
northern Simi Hills (BLUNDELL, 1983); upper Sespe Creek, 
Ventura County (herein); western Santa Ynez Mountains, 
Santa Barbara County (LOEL & Corey, 1932); tentatively 


Page 401 


the Eagle Rest Peak area, San Emigdio region, southern 
Kern County, south-central California (LOEL & CoREy, 
1932); and tentatively the Vaqueros Creek area, Junipero 
Serra Peak region, Monterey County, north-central Cal- 
ifornia (LOEL & Corey, 1932). 


Remarks: A total of 340 specimens were seen during the 
course of this study. The holotype (Figures 3-6) is the best 
preserved specimen, but it is the only specimen that has a 
body whorl narrower than the penultimate whorl. The 
holotype also shows the central plait in the aperture better 
than any other specimen. Figure 4 illustrates the coinci- 
dence of this central plait with the columellar side of the 
anterior canal. The columellar callus is fairly well devel- 
oped on the holotype, but the specimen illustrated in Figure 
7 shows how pronounced this callus can be. The presence 
of a detached columellar callus helps to determine that this 
species is a certhiid rather than a terebrid. In addition, the 
lack of a siphonal fasciole on Clavocerithium (C.) santanum 
further underscores that the species is not a terebrid, as 
all members of family Terebridae have a siphonal fasciole 
(BRATCHER & CERNOHORSKY, 1987). 

The holotype is the only specimen that shows growth 
lines. These are readily discernible in Figures 3-5, and 
Figure 5 illustrates the sinuous outer lip. The whorls on 
the holotype are tabulate. A few specimens have convex 
whorls (Figure 7), and others are transitional (Figure 8) 
between convex whorls and prominently tabulate whorls 
(Figure 9). Variation in shell form is common in species 
of cerithiids (HouBRICK, 1978; Kay, 1979), and well-il- 
lustrated examples are shown in Housrick (1978:pls. 2, 
13, 16, 94). His plate 94 shows examples of variation of 
shell form in Clavocerthium. 

Nearly every observed specimen of Clavocerithium (C.) 
santanum is smooth over the entire shell. At locality LAC- 
MIP 7700, however, several partial specimens that consist 
of the middle part of the spire show faint traces of spiral 
ribbing on the spire whorls. One of these specimens (Figure 
10) shows four spiral ribs. The spiral rib in the sutural 
area is, in most cases, the only spiral rib that is preserved 
(Figure 11). Abrasion of shell sculpture, therefore, is a 
major factor in the studied specimens. The abrasion may 
have taken place during post-mortem transport by waves 
and/or currents. 

No specimens of Clavocerithium (C.) santanum were found 
that show any traces of spiral or axial ribbing on the 
exteriors of the more anterior spire whorls or on the body 
whorl. These whorls are judged to have originally been 
smooth. The presence of growth lines on the penultimate 
and body whorls of the holotype suggest that this particular 
specimen underwent minimal post-mortem transport, oth- 
erwise the growth lines would have been worn off. The 
whorls of this specimen show no spiral ribbing or other 
external ornamentation. 

It is also possible that hermit crabs could have lived in 
the shells. Modern certhiid shells commonly serve as homes 
for hermit crabs. For example, dead specimens of Cer- 


Page 402 


The Veliger, Vol. 36, No. 4 


Explanation of Figures 3 to 12 


Figures 3-12. Clavocerithium (C.) santanum (Loel & Corey, 1932). Figures 3-6: holotype UCMP 31608, locality 
UCMP 6128, apertural, oblique apertural, lateral, and abapertural views, <3.8; Figure 7: hypotype LACMIP 
12103, locality LACMIP 7700, oblique apertural view, x 3.1; Figure 8: hypotype LACMIP 12104, locality CSUN 
1185, apertural view, x 2.6; Figure 9: hypotype LACMIP 12105, locality CSUN 1185, abapertural view, x 3.3; 
Figure 10: hypotype LACMIP 12106, locality LACMIP 7700, abapertural view of middle spire, x3.1; Figure 
11: paratype UCMP 31611, locality UCMP A-252, apertural view, x 2.9; Figure 12: hypotype LACMIP 12107 


locality, LACMIP 7700, apertural view, x 3.5. 


thium stercusmuscarum in the northern Gulf of California 
are commonly inhabited by hermit crabs (HARTSHORNE et 
al., 1987; FURISCH & FLEssA, 1987). Nearly all the spec- 
imens that I observed of this gastropod on the tidal sandflat 
at San Felipe were occupied by hermit crabs. Some of the 
abrasion of the shells of Clavocerithium (C.) santanum could 
have taken place during movements associated with the 
hermit crabs. 

Only about 15% of the studied specimens of Clavocer- 
thium (C.) santanum have retained their apertures, and 


only a few of these specimens show the fragile outer lip, 
the very fragile detached columellar callus, and the central 
plait on the columella. These features, especially the cen- 
tral plait on the columella, could have been worn off if the 
shells served as homes for hermit crabs. 

Most of the specimens of Clavocerithium (C.) santanum 
that are in the LACMIP collection from locality LACMIP 
7700 consist only of the upper spire. Many of these are 
like other specimens of this species found elsewhere in that 
the upper spire whorls are straight sided for the first 3 to 


R. L. Squires, 1993 


6 mm in height and grade into tabulate whorls beyond 
that height. On a few specimens from locality 7700, how- 
ever, the upper spire whorls remain straight sided for up 
to 15 mm in height (Figure 12), and the rest of the shell 
(presumably with tabulate whorls) is missing. Specimens 
with such long and slender upper spire whorls were de- 
tected only at this locality. 

Previously, Clavocerithium (Clavocerithium) comprised 
only C. (C.) lacazei (COSSMANN, 1897:pl. 11, figs. 15, 17; 
1898:15; 1920:94-95, pl. 3, figs. 24-25; WENz 1940:762, 
fig. 2208; Housrick, 1978:121, pl. 93, figs. 1, 2) from the 
upper? Eocene at Bois Gouét, Brittany, northwestern 
France. The exact age of these fossil beds has been much 
disputed, and assigned by various authors to either the 
middle Eocene or late Eocene (DAVIES, 1975:186). 

On the basis of comparisons with several LACMIP 
specimens of Clavocerithium (C.) lacazei from Bois Gouet, 
as well as with the published illustrations of this species, 
C. (C.) santanum differs in having (1) a smaller shell, (2) 
whorls more tabulate (although a few specimens have con- 
vex whorls similar to those in C. (C.) lacazez, (3) four 
rather than 12 spiral ribs on middle of spire, (4) a detached 
columellar callus, (5) no axial ridges on upper whorls, and 
(6) a columellar callus that is not just restricted to the 
parietal area. 

Clavocerithium (Clavocerithium) santanum, which is only 
the second species in the typical subgenus, is the first report 
of this subgenus in the New World, fossil or Recent, and 
the first early Miocene report. 

Indocerithium Chavan, 1952, is the only other known 
subgenus of Clavocerithium. HOUBRICK (1975, 1978) re- 
viewed Indocerithium, which is distinguished by an outer 
lip that extends one-third onto the previous whorl, and 
reported the subgenus to range from early Pliocene to 
Recent. Only three species are assigned to this subgenus, 
and two are extinct. All are from Indonesia and/or the 
Philippines and are associated with coral-reef biotopes. 

The name Clavocerithium is a Latin neuter noun, and 
the species name santana must be changed to santanum. 


ACKNOWLEDGMENTS 


David R. Lindberg and Rex A. Hanger (University of 
California Museum of Paleontology, Berkeley) provided 
for the loan of the primary type material. LouElla R. Saul 
(Natural History Museum of Los Angeles County, In- 
vertebrate Paleontology Section) and Marilyn Kooser 
(University of California, Riverside) allowed access to col- 
lections and provided for loans. Lindsey T. Groves (Nat- 
ural History Museum of Los Angeles County, Malacology 
Section) allowed access to Recent collections of mollusks. 

Clif Coney, Lindsey T. Groves, and James H. McLean 
(Natural History Museum of Los Angeles County, Mal- 
acology Section), George L. Kennedy and LouElla R. Saul 
(Natural History Museum of Los Angeles County, In- 
vertebrate Paleontology Section), and Twila Bratcher 
(Hollywood, California) gave valuable comments regard- 
ing identifications. 


Page 403 


Bruce Lander (Paleo Environmental Associates) and 
Barbara Parkhurst (George C. Page Museum, Los An- 
geles) provided paleontological contacts for the Orange 
County area. Steve Conkling (Ralph B. Clark Interpre- 
tative Center, Orange County) and John Minch (Envi- 
ronmental Resource Investigations) provided information 
about access to Trabuco Canyon. Ginny McVickar (O’Neill 
Regional Park, Orange County) allowed access into Tra- 
buco Canyon. 

Ellen J. Moore (Corvallis, Oregon) and an anonymous 
reviewer gave valuable comments. 


LOCALITIES CITED 


CSUN 159. SW ¥Y, of section 36, TON, R22W, U.S. Geo- 
logical Survey, 7.5-minute, Lion Canyon, California 
Quadrangle, 1943, upper Sespe Creek area, Ventura 
County, southern California (SQUIRES & FRITSCHE, 
1978:fig. 2B). 

CSUN 401. SW ¥Y, of section 33, TON, R21W, U.S. Geo- 
logical Survey, 7.5-minute, Topatopa Mountains, Cal- 
ifornia Quadrangle, 1943, upper Sespe Creek area, 
Ventura County, southern California (SQUIRES & 
FRITSCHE, 1978:fig. 2C). 

CSUN 428. In extreme NW corner of section 26, TON, 
R22W, U.S. Geological Survey, 7.5-minute, Lion Can- 
yon, California Quadrangle, 1943, upper Sespe Creek 
area, Ventura County, southern Caifornia (SQUIRES & 
FRITSCHE, 1978:fig. 2B). 

CSUN 555. NE ‘4 of the SW ¥, of section 20, T3N, R 
18W, U.S. Geological Survey, 7.5-minute, Simi, Cali- 
fornia Quadrangle, 1943, Big Mountain, north side of 
Simi Valley, Ventura County, southern California 
(BLUNDELL, 1981:pl. 1). 

CSUN 1185. Along steep ridge, at elevation of 860 ft. (265 
m), near head of Hicks Canyon, *’33100 m N and 
434700 m E (1000-meter Universal Transverse Mer- 
cator Grid, 1927 datum), U.S. Geological Survey, 7.5- 
minute, El Toro, California Quadrangle, 1968 (pho- 
torevised 1982), northern Santa Ana Mountains, 
Orange County, southern California (DANIEL, 1989: 
appendices B2 and C4). 

LACMIP 7700. Cliff west of old adobe in SW part of 
Plano Trabuco, N40°W of old adobe, 34 m above stream 
bench in 1-m-thick bed of hard ledge-forming slimy 
sandstone, in places almost a coquina (LACMIP rec- 
ords), U.S. Geological Survey, 7.5-minute, Canada 
Gobernadora, California Quadrangle, 1968 (photore- 
vised 1988), southern end of northern Santa Ana Moun- 
tains, Orange County, southern California. 

UCMP 6128. “At base of bluff, west of the S end of the 
remnant hill which is on the lower plain, west side of 
Plano Trabuco” (LOEL & Corey, 1932:57), U.S. Geo- 
logical Survey, 7.5-minute, Canada Gobernadora, Cal- 
ifornia Quadrangle, 1968 (photorevised 1988), southern 
end of northern Santa Ana Mountains, Orange County, 
southern California. 

UCMP A-253. “N side of first large gulch on E side of 


Page 404 


Wiley Canyon, center of S side of section 36, T4N, 
R19W, lowest invertebrate fossilferous bed (possibly 
estuarine deposition)” (LOEL & Corey, 1932:79), south 
side of Santa Clara River, Oak Ridge area, U.S. Geo- 
logical Survey, 7.5-minute, Piru, California Quadran- 
gle, 1952 (photorevised 1969), Ventura County, south- 
ern California. 


LITERATURE CITED 


BADGER, R. L. 1957. Geology of the western Lion Canyon 
quadrangle, Ventura County, California. Unpublished 
Master of Arts Thesis, University of California, Los Angeles. 
84 pp. 

BLUNDELL, M.C. 1981. Depositional environments of the Va- 
queros Formation in the Big Mountain area, Ventura Coun- 
ty, California. Unpublished Master of Science Thesis, Cal- 
ifornia State University, Northridge. 102 pp. 

BLUNDELL, M.C. 1983. Depositional environments of the Va- 
queros Formation, Big Mountain area, Ventura County, 
California Pp. 161-172. In: R. L. Squires & M. V. Filewicz 
(eds.), Cenozoic Geology of the Simi Valley Area, Southern 
California. Pacific Section, Society of Economic Paleontol- 
ogists and Mineralogists, Volume and Guidebook No. 35. 

BRATCHER, T. & W. CERNOHORSKY. 1987. Living Terebras 
of the World. American Malacologists: Melbourne, Florida. 
240 pp., 68 pls. 

Brusca, R. C. 1980. Common Intertidal Invertebrates of the 
Gulf of California. 2nd ed. The University of Arizona Press: 
Tucson, Arizona. 513 pp. 

CHAVAN, A. 1952. Quelques intéressantes types de cérithes. 
Cahiers Geologiques de Thoiry, No. 12:103-104. 

CossMANN, M. 1897. Mollusques éocéniques de la Loire-In- 
férieure. Bulletin de la Société des Sciences Naturelles de 
Ouest de la France (Nantes), Série 1, 7:297-358, pls. 5- 
10 

CossMANN, M. 1898. Mollusques éocéniques de la Loire-In- 
férieure. Bulletin de la Société des Sciences Naturelles de 
Ouest de la France (Nantes), Série 1, 8:1-55, pls. 1-3. 

CossMANN, M. 1920. Supplement aux mollusques éocéniques 
de la Loire-Inférieure. Bulletin de la Société des Sciences 
Naturelle de ’OQuest de la France (Nantes), Série 3, 5:53- 
141, pls. 1-4. 

DanigEL, L. L. 1989. Stratigraphy and depositional environ- 
ments of the lower Miocene Vaqueros Formation, Santa Ana 
Mountains, California. Unpublished Master of Science The- 
sis, California State University, Northridge. 100 pp. 

Davigs, A. M. 1975. Tertiary Faunas—A Text-book for Oil- 
field Palaeontologists and Students of Geology. Vol. 2, The 
Sequence of Teritary Faunas, Revised by F. E. Eames & 
R. J. G. Savage. George Allen & Unwin: London. 447 pp. 

FLEMING, J. 1822. The Philosophy of Zoology; or a General 
View of the Structure, Functions and Classification of An- 
imals. 2 Vols. Edinburgh. 1050 pp. 

Fursicu, F. T. & K. W. FLEssa. 1987. Taphonomy of tidal 
flat molluscs in the northern Gulf of California: paleoen- 
vironmental analysis despite the perils of preservation. Pp. 
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California. The Paleontological Society Special Publication 
No. 2. 

HARTSHORNE, P. M., W. B. GILLESPIE & K. W. FLESSA. 1987. 
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little-known and unusual cerithiid from New Guinea. The 
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Pacific. Part 1: The genera Rhinoclavis, Pseudovertagus and 
Clavocerithium. Monographs of Marine Mollusca, No. 1. 
130 pp., pls. 1-98. 

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California Publications, Bulletin of the Department of Geo- 
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REID, S.A. 1978. Mid-Tertiary depositional environments and 
paleogeography along upper Sespe Creek, Ventura County, 
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ecology and Taphonomy of Recent to Pleistocene Intertidal 
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Special Publication No. 2. 

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KINNEY. 1981. Geology of the northern Santa Ana Moun- 
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sional Paper 420-D. 109 pp. 

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along Sespe Creek, Ventura County, California. Pp. 6-26, 
pls. 1-4. In: A. E. Fritsche (ed.), Depositional Environments 
of Tertiary Rocks Along Sespe Creek, Ventura County, Cal- 
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VALENCIENNES, A. 1932. Coquilles marines univalves de 
P?Amerique Equinoxial, recuillies pendent le voyage de MM. 
de Humboldt et Bonpland. Pp. 262-239, pl. 57. In: F. H. 
A. von Humboldt & A. J. A. Bonpland, Voyage aux regions 
equinoxiales du Noveau Contient. Paris, Pt. 2, Recuer] d’ob- 
servations de zoologie et d’anatomie comparee 2 (Pt. 2). 

WENZ, W. 1940. Superfamilia Cerithiaceae. Pp. 650-787. In: 
O. H. Schindewolf (ed.), Handbuch der Paldozoologie, Band 
6, Prosobranchia, Teil 4. Gebriider Borntraeger: Berlin [re- 
printed 1960-1961]. 


The Veliger 36(4):405-412 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


The Validity of Chaetoderma montereyense Heath 


Along with Ch. argenteum Heath 


(Mollusca: Caudofoveata) 


by 


LUITFRIED v. SALVINI-PLAWEN 


Institut of Zoology, University of Vienna, A-1090 Wien IX., Austria, Althanstr. 14 


Abstract. 


The northeastern Pacific aplacophoran mollusk species Chaetoderma argenteum, Ch. atten- 


uatum, and Ch. montereyense (Caudofoveata), diagnosed by HEATH (1911) and recently synonymized 
as a single species Ch. argenteum Heath, are reexamined. Detailed analysis of the type material reveals 
(1) that Heath’s description of Ch. attenuatum refers to a specimen of Ch. montereyense, and (2) that 
Ch. attenuatum is anatomically (pericardium and other characters) and geographically (Alexander 
Archipelago, south Alaska) identical with Ch. argenteum only. Thus, Ch. attenuatum can be synonymized 
with Ch. argenteum, whereas Ch. montereyense (off Santa Barbara, California to Vancouver, B.C.) is to 


be maintained as a valid species. 


INTRODUCTION 


HAROLD HEATH (1911) described the aplacophoran 
Mollusca (‘‘Solenogastres”)—1.e., the Solenogastres proper 
(= former Neomeniomorpha) as well as the separated 
Caudofoveata (= former Chaetodermomorpha)—of an ex- 
pedition in 1899-1900 to the tropical Pacific. Whereas the 
Solenogastres proper are adequately presented, the de- 
scriptions of the Caudofoveata (viz. Chaetoderma and Lim- 
ifossor) are in part scanty. This has caused some difficulties 
in specific identification (cf. STORK, 1941:55; SAL- 
VINI- PLAWEN, 1972:228, 1992; SCHELTEMA et al., 1991), 
especially concerning the species diagnosed by Heath as 
Chaetoderma attenuatum and Ch. montereyense'). 

In their recent paper, SCHELTEMA et al. (1991) consid- 
ered specific identity not only of those two nominal species 
(not really different according to Heath; see also STORK, 
1941:55), but they declared both to be junior synonyms of 
Chaetoderma argenteum HEATH, 1911. With respect to Ch. 
argenteum, however, there are differences described by 
Heath. Within the general organization of the Caudofov- 
eata (see SALVINI- PLAWEN, 1985, for a detailed account), 


' The generic name Chaetoderma is of neuter gender (see also 
Opinion 764 in the Bulletin of Zoological Nomenclature 23(1):22 
(1966)). Consequently, as already done in SALVINI- PLAWEN 1972: 
380, all species need neuter endings (in contrast to HEATH’s 
(1911) original spellings): Article 34b of the ICZN. 


the present contribution points out these differences based 
on an anatomical analysis and evaluates them with respect 
to conspecifity. 


THE MATERIAL CONCERNED 


(1) H. Heath described the new species Chaetoderma 
argentea (correctly: argenteum) on the basis of a single, 24- 
mm-long specimen. This was collected at Albatross Sta. 
4231 in 82-113 fms (150-207 m) from the Alexander 
Archipelago in south Alaska, near Naha Bay in the Behm 
Canal (55°59'N, 131°17’W; HEATH, 1911:9, 62). This type 
is deposited in the California Academy of Sciences as a 
slide series CAS no. 190 (STASEK, 1966:2). 

(2) The description of Chaetoderma attenuata (correctly: 
attenuatum), likewise from the Alexander Archipelago in 
south Alaska, by HEATH (1911:9, 43, 55-59) was based 
on a total of eight individuals (not “16” specimens as 
incorrectly indicated by STASEK, 1966:2) measuring up to 
61 mm in length. Five specimens came from Albatross Sta. 
4250 (Simonof Island, opposite the mouth of the Stikine 
River, about 56°42'’N, 132°25'W, at 61-66 fms = 87-94 
m depth), one individual from Sta. 4244 (Kasaan Bay of 
Clarence Strait, at the eastern coast of Prince of Wales 
Island, 55°30'N, 132°25'W, at 50-54 fms = 91.5-98 m) 
and two specimens from the geographically more distant 
Sta. 4252 (Stephens Passage at 198-201 fms = 360-368 
m depth). HEATH definitely speaks of a type specimen 
(1911:55) which, bona fide in agreement with STASEK (1966: 


Page 406 


The Veliger, Vol. 36, No. 4 


Figure 1 


Body regions in the Caudofoveata-Chaetodermatidae. 1, peribuccal region; 2, region of foregut; 3, region of midgut 
(anterior trunk); 4, region of midgut sac (posterior trunk); 5, prepallial region (of gonopericardial ducts); 6, region 
of pallial cavity (after SALVINI-PLAWEN, 1975). The Chaetoderma species treated here correspond to the regionation 


in “A” (see also SCHELTEMA et al., 1991:fig. 1). 


2), is identical with the sectioned animal CAS no. 191. 
Other material is kept as paratypes by the MCZ at Har- 
vard University (see also SCHELTEMA et al., 1991:table 1). 
At present they include four specimens from Sta. 4250, 
the single individual from Sta. 4244, and the two specimens 
from Sta. 4252. The individual from Sta. 4244 is preserved 
together with two specimens from Sta. 4250 (one individ- 
ual without a posterior body portion and two specimens 
lacking the foregut region; one animal of this mixed sam- 
ple, a fragment of 40 mm, has been used here to prepare 
serial sections of the posterior body, see below). Thus, 
seven individuals (in part being incomplete) are retained 
in alcohol, and the eighth specimen had been used for the 
series section (CAS no. 191). 

(3) A third Chaetoderma species from the Alexander 
Archipelago had been described by HEATH (1911:9, 43, 
59-61) as CA. erudita (correctly: eruditum). Ten specimens 
of up to 27 mm in length were taken in the Lynn Canal 
at 300-313 fms (549-573 m) depth (Albatross Sta. 4258) 
and 41 individuals came from the Chatham Strait at 282- 
293 fms (516-536 m) depth (Sta. 4264). This material 
(paratypes; holotype = ?) is held in the MCZ at Harvard 
University. 

(4) Among the species described by Heath from off 
California, Chaetoderma montereyensis (correctly: monter- 
eyense) was represented by 181 specimens. They measure 
up to 45 mm in length and stem from eight stations (nos. 
4485, 4508, 4510, 4522, 4523, 4524, 4525, 4526) at 39- 
356 fms (71-642 m) depth in Monterey Bay (HEATH 1911: 
9, 43, 61; supplemented in SCHELTEMA et al., 1991:table 
1). No type was designated by HEATH (1911), but one of 
the above 181 syntypes is maintained as a series section 
on slides (CAS no. 194). This is herein designated as the 
lectotype, rather than a syntype (STASEK, 1966:3) or the 
holotype (SCHELTEMA et al., 1991:table 1). 


COMPARATIVE ANALYSIS 


As was the case with several other descriptions of Cau- 
dofoveata by HEATH (1911), the diagnostic characters of 
the four nominal species in question are also only scantly 
elaborated. Generally, a detailed analysis of the sequence 
of the mantle scales along the regionated body (Figure 1) 
will reveal specific differences (cf. SALVINI- PLAWEN, 1978); 
in the present case, no such detailed representation of the 
spicules exists. The illustration of the aragonitic body scales 
by HEATH (1911:pl. 37) is similar for all Chaetoderma 
species and is thus not truly informative. SCHELTEMA et 
al. (1991:fig. 3A) provide camera lucida drawings of CA. 
argenteum spicules that are very similar to those of Ch. 
montereyense. On the other hand, the present author also 
examined the mantle scales of four paratypes of Ch. eru- 
ditum Heath (HEATH, 1911:Stat. 4258, 4264); the bent 
spicules in the midgut region (cf. also HEATH, 1911:pl. 
37, fig. 15) resemble those of the above-named species. 
Other spicules of Ch. eruditum, however, are distinctly 
different (e.g., in the region of the midgut sac: Figure 2). 
Thus, Chaetoderma eruditum Heath is well-diagnosed by 
its spicules alone and can be excluded from the present 
discussion. 

In May 1966, several Chaetoderma samples from Puget 
Sound were submitted by K. Banse (University of Wash- 
ington, Seattle) to the present author. Based on the de- 
scription by HEATH (1911), several specimens represent 
either Chaetoderma montereyense or Ch. attenuatum. The 
body cover (mantle scales) is almost identical in paratypes 
of both nominal species (see Figures 3, 4). Based on the 
mantle scales, three additional specimens from Puget Sound, 
Seattle, Washington sent in 1979 to the present author by 
F. Nichols (U.S. Geological Survey, Menlo Park, Cali- 
fornia), were likewise identified (February, 1980) as Ch”. 


L. v. Salvini-Plawen, 1993 Page 407 


4007pm 


{edt 


Sequence of mantle scales in Chaetoderma eruditum Heath (paratype Sta. 4258). a-d, foregut region; e-i, midgut 
region; k-m, region of midgut sac; n-o, prepallial and pallial regions. 


Figure 2 


300 pm 


a 
fiiasbhdl 


Figure 3 


Sequence of mantle scales in Chaetoderma montereyense Heath (paratype Sta. 4526). a—b, foregut region; c-i, midgut 
region; k—n, region of midgut gland; o-p, prepallial and pallial regions; q, bordering the dorsoterminal sense organ. 


Page 408 


3007 pm 


7NMA badd 


The Veliger, Vol. 36, No. 4 


Figure 4 


Sequence of mantle scales in Chaetoderma attenuatum Heath (paratype Sta. 4250). a—b, foregut region; c-i, midgut 
region; k-n, region of midgut sac; o-p, prepallial and pallial regions; q, bordering the dorsoterminal sense organ. 


montereyense. SCHELTEMA et al. (1991) presented recent 
findings of Chaetoderma material from Point Conception, 
California, to Vancouver Island, British Columbia (see 
also BUCKLAND-NICKS & CHIA, 1989). The animals belong 
to Ch. montereyense Heath (as already hinted by the present 
author to Buckland-Nicks in a letter on 26 January 1990), 
a species which SCHELTEMA et al. (1991), mainly due to 
the similarity of the mantle scales, synonymized not only 
with Ch. attenuatum but also with Ch. argenteum. Contrary 
to the opinion of SCHELTEMA et al. (1991:208) that HEATH 
(1911) “did not differentiate C. argenteum, C. attenuata, 
and C. montereyensis either by written description or by 
illustration,” there are described differences as concerns 
Ch. argenteum (cf. HEATH, 1911; see below). Thus, a re- 
examination of the series-sectioned type material of the 
three nominal species was undertaken in order to clarify 
the discrepancies between Heath’s description and the above 
synonymization. In addition, Dr. K. Boss (Curator at the 
MCZ, Harvard) permitted the posterior end of one CA. 
attenuatum paratypes to be series sectioned. 

The detailed anatomical comparison of all three nominal 
species revealed a far-reaching identity in internal orga- 
nization (for exceptions, see below). Beside the general 
similarity of the mantle scales (Figures 3, 4; see also 
SCHELTEMA et al., 1991), they also share the pedal shield 
with an anterior oral cleft (according to the type series of 
Chaetoderma argenteum; HEATH, 1911:56 and personal ob- 
servation for Ch. attenuatum; personal observation and 
SCHELTEMA et al., 1991, for Ch. montereyense, in contrast 
to HEATH, 1911:1.4, figs. 14, 17). The foregut with its 


glands, as well as the radula apparatus, coincide (in Ch. 
montereyense the latter is not “exceptionally heavy and 
powerful” as described by HEATH, 1911:62, but merely in 
a different state of contraction). The different size of the 
radular basal cone may reflect relative body size (300 x 
100 um in Ch. argenteum, up to 500 x 200 um in CA. 
attenuatum, and up to 500 x 175 um in CA. montereyense). 
There are six pairs of precerebral ganglia and a dorso- 
posterior lobus impar joining the cerebral ganglia (Sa- 
LVINI- PLAWEN, 1972:298); the posterior nervous system is 
almost identical, including the ventral ctenidial nerves (= 
the so-called subrectal commissure of WIREN, 1892:taf. VII, 
fig. 3) emerging ventrally from the suprarectal ganglionic 
mass. All three nominal species show a strong, more or 
less separated lateral muscle bundle along both sides of 
the foregut-anterior midgut. For comparison, this paired 
bundle represents a specific character of Ch. nitidulum 
Loven, in contrast to Ch. canadense Nierstrasz (where it 
is missing; cf. SALVINI- PLAWEN, 1988:308). 

In general, two pairs of retractors from the efferent side 
of the ctenidia (posteriodorsal and anteriodorsal bundles 
which mostly pass the pericardium) and two pairs of af- 
ferent ctenidial retractors (lateral and ventral bundles) 
exist. They show individual variability in strength, but the 
ventral retractors are the strongest; in Scutopus ventroli- 
neatus Salvini-Plawen the latter continue into the m. lon- 
gitudinalis and enable the body to roll up. Incomplete or 
complete subdivision may result in five pairs (e.g., in S. 
ventrolineatus; cf. also WIREN, 1892; see Figure 5 herein) 
or even six pairs (e.g., in Prochaetoderma californicum 


L. v. Salvini-Plawen, 1993 


Page 409 


Figure 5 


Arrangement of musculature in the posterior body of Caudofoveata. A. Cross section along line A-A in B. B. Lateral 
projection. at, atrium of heart; bwm, body wall musculature; co, ganglionic suprarectal commissure; ct, ctenidium; 
dts, terminal sense organ; gd, glandular duct; int, intestine; mgs, midgut sac; ns, fused lateral/ventral nerve cord; 
pc, pericardium; rda, anteriodorsal retractor; rdp, posteriodorsal retractor; rl, lateral retractor; rva, anterioventral 
retractor; rvp, posterioventral retractor; sph, terminal sphincter of the pallial cavity. 


Schwabl; cf. also SCHWABL, 1963). In all three nominal 
species treated here, four pairs of ctenidial retractors are 
present as in Chaetoderma canadense or Ch. intermedium 
Knipowitsch (personal observation). The ventral retractors 
show a posterior portion which, however, is not separated; 
the posteriodorsal retractors insert at the basi-ctenidial 
wall of the mantle cavity. 

The heart runs freely within the pericardium and bears, 
at the anterior end of the latter, a middorsal opening. 
Anterior to the aortal bulbus, the vessel continues as an 
aorta within the lumen of the gonopericardioduct and with- 
in the posterior portion of the fused gonad; the gonoper- 
icardioduct itself is unpaired, laterally and/or ventrally 
ciliated and has sporadic ventral and/or dorsal connecting 
suspensions of the aorta. The pericardial outlets, composed 
on each side of two sections, viz. a ciliated pericardioduct 
and a spacious glandular duct, are of identical outline in 
the three nominal species: the pericardioducts are very 
short and open directly into the upper dorsoposterior limb 
of the U-shaped glandular ducts, as correctly described 
and illustrated by HEATH (1911) for Ch. argenteum only 
(see Figure 8). 

Despite all these coincidences, however, distinct differ- 
ences exist: 


(1) In Chaetoderma argenteum, (a) the spicules preserved 
with the type CAS no. 190 (slide 92) fit into the con- 
figurations of the elements in the two other nominal 
species without marked differences (cf. SCHELTEMA et 
al., 1991:fig. 3). Due to the single, sectioned specimen, 
no further reexamination is possible. (b) As is illus- 


(2 


a 


trated by HEATH (1911:pl. 26, fig. 5; pl. 36. fig. 1), 
there is no extension of the pericardium beyond the 
beginning of the pallial cavity. (c) The ventral, lateral, 
and anteriodorsal ctenidial retractors are paired and 
of usual elaboration. (d) The posteriodorsal ctenidial 
retractors represent an unpaired bundle (see Figure 
6) that splits only upon reaching the dorsal body wall. 
(e) The buccal connective branches off at each side of 
the common trunk (of connectives from the cerebral 
ganglion) fairly early at a distance of 120 um. (f) The 
recorded locality is the Behm Canal in the south- 
western Alexander Archipelago (south Alaska). 

In Chaetoderma montereyense, (a) the spicules (gi) in 
Figure 3 (= scales ‘4 in SCHELTEMA et al., 1991:fig. 
3D) appear to be dominant in the posterior midgut 
region. (b) As described by HEATH (1911:62), the 
“pericardium is a comparatively spacious chamber,” 
extending behind the heart broadly backward some 
distance over the mantle cavity; this is also correctly 
illustrated (HEATH, 1911:pl. 27, fig. 9). (c) Although 
the ventral, lateral, and anteriodorsal pairs of ctenidial 
retractors are elaborated as usual, there is an addi- 
tional (lateral) bundle on the right side (Figure 7 77); 
it originates together with the right lateral retractor 
and inserts at the hindgut as illustrated by Heath (see 
Figure 7, herein). (d) The posteriodorsal ctenidial re- 
tractors begin as a paired bundle which fuses at the 
level of the pericardium (cf. HEATH, 1911:pl. 27, fig. 
8) and splits again upon reaching the middorsal body 
wall (Figure 7). (e) The buccal connective splits off 
the common trunk at a distance of 200 um. 


Page 410 


The Veliger, Vol. 36, No. 4 


Explanation of Figures 6 and 7 


Figure 6. Cross section through heart and glandular ducts of 
Chaetoderma argenteum, taken from HEATH (1911:pl. 26, fig. 3). 
cp, glandular duct; ns, fused lateral/ventral nerve cord; pc, peri- 
cardium; rda and rdp, anteriodorsal and posteriodorsal ctenidial 
retractors; rl, lateral ctenidial retractor; rv, ventral ctenidial re- 
tractor. 


These characters of the lectotype (a female) corre- 
spond exactly with the sectioned Puget Sound, Seattle 
(1966) specimen (a male). The characters are unre- 
lated to different body sizes, for example with respect 
to the length of the common trunk of connectives. Some 
scales are present, however, which correspond to the 
spicule ‘i’ in Figure 4, and the asymmetrical muscle 
bundle at the hindgut is less prominent. (f) The geo- 
graphical distribution thus clearly includes Monterey 
Bay, California (type material), and Puget Sound, 
Washington, but probably ranges from Point Concep- 
tion, California, to Rainy Bay, off SW Vancouver 
Island, southern British Columbia (BUCKLAND-NICKS 
& CHIA, 1989; SCHELTEMA et al., 1991). 

(3) The description of Chaetoderma attenuatum by HEATH 
(1911:55-59) largely corresponds to that of Ch. mon- 
tereyense (STORK, 1941:55; SALVINI-PLAWEN, 1972: 
228; SCHELTEMA et al., 1991). The coincidence also 
includes the pericardium, which “‘is of unusual size, 
extending behind the heart nearly to the posterior end 
of the body” (HEATH, 1911:58, also pl. 25, fig. 5, and 
pl. 36, fig. 2). This specimen is a female as evidenced 
by the mucous tracts (“glandular epithelium”’) in the 
ventral mantle cavity (HEATH, 1911:58, and drawn in 
fig. 5 of pl. 25). 

This description, however, does not correspond to 
the type material! (a) Spicules of paratypes show dif- 
ferences in their dominance in the posterior midgut 


Figure 7. Cross section through heart and glandular ducts of 
Chaetoderma montereyense, taken from HEATH (1911:pl. 27, fig. 
2). ep, glandular duct; int, intestine; ns, fused lateral/ventral 
nerve cord; pc, pericardium; rda and rdp, anteriodorsal and pos- 
teriodorsal ctenidial retractors; rl, lateral ctenidial retractor; rr, 
ctenidial retractor to hindgut; rv, ventral ctenidial retractor. 


region (Figure 4g-i) when compared with Chaetoder- 
ma montereyense. The sole series-sectioned individual 
of Ch. attenuatum (holotype, CAS no. 191) is a male 
and its anatomy points to Ch. argenteum. (b) The 
pericardium does not extend beyond the beginning of 
the mantle cavity. (c) Among the ctenidial retractors 
there is no particular retractor to the hindgut (merely 
the left lateral retractor is bipartite). (d) The posterio- 
dorsal ctenidial retractor is largely unpaired. (e) The 
buccal connective emerges after a short distance of 80- 
120 wm. And (f) the animals originate from the Al- 
exander Archipelago, south Alaska. Yet, the posterior- 
most body is ventrally bent and hence obliquely sec- 
tioned (and in no way corresponds to figs. 4, 5, and 8 
of pl. 25 in HEATH, 1911); in addition, this part is in 
poor histological condition. Consequently the posterior 
body of a paratype of the above-mentioned mixed sam- 
ple had been series sectioned for certainty: this spec- 
imen either originated from the type locality (Sta. 4250, 
off Simonof Island) or it represents the single individ- 
ual from the sample Sta. 4244 (Kasaan Bay of Clar- 
ence Strait), which is closest to the type locality of Ch. 
argenteum. Its anatomy (a male in moderate histolog- 
ical condition) likewise fully coincides with the specific 
characters of Ch. argenteum (pericardium, ctenidial 
retractors) but not with Ch. montereyense. The differ- 
ence in body size, 24 mm CA. argenteum versus more 


L. v. Salvini-Plawen, 1993 


Page 411 


Explanation of Figures 8 and 9 


Figure 8. Reconstruction of posterior end of Chaetoderma argen- 
teum, taken from HEATH (1911:pl. 36, fig. 1). cp, glandular duct; 
dts, terminal sense organ; hg, hindgut; ht, heart; pc, pericardium. 


than 40 mm of the sectioned Ch. attenuatum paratype, 
is of no relevance for the anatomical configuration. 


DISCUSSION 


The Caudofoveata are animals having a fairly uniform 
organization (see SALVINI-PLAWEN, 1985 for a general 
outline), and classification at the species level may cause 
difficulties. Generally, differences in the sequence of the 
mantle scales (size, outline, structure) are sufficient to de- 


Figure 9. Reconstruction of posterior end (without ctenidium) of 
Chaetoderma dict. ‘“‘attenuatum,” taken from HEATH (1911:pl. 36, 
fig. 2). cp, glandular duct; dts, terminal sense organ; hg, hindgut; 
ht, heart; pc, pericardium. 


fine a species. In cases where such differences may not be 
distinct enough, additional characters are needed. This is 
true for the chaetodermatids Falcidens chiastos Scheltema 
(1989) and F. targotegulatus Salvini-Plawen (1992), the 
latter being also defined by its perioral pedal shield. Sim- 
ilarly, Chaetoderma canadense Nierstrasz and Ch. nitidulum 
Loven are distinguished by scales, the radula apparatus, 
and the presence of the paired lateral muscles bundle along 
the anterior midgut (SALVINI-PLAWEN, 1975:43; 1978; 


Page 412 


1988:308 versus SCHELTEMA et al., 1991:212). In addition, 
Ch. nitidulum elaborates a (proximally paired) posterio- 
dorsal ctenidial retractor, which splits into four bundles 
(WIREN, 1892, and personal observations), whereas the 
posteriodorsal retractor in CA. canadense is unpaired-fused 
and does not split before reaching the middorsal body wall 
(personal observations); in Ch. intermedium Knipowitsch 
this retractor emerges paired, but continues fused-unpaired 
and enters the body wall musculature again as a paired 
bundle. 

In contrast to the almost identical scales of Chaetoderma 
argenteum and Ch. montereyense, the listed differences are 
of species-specific significance. Especially pericardium and 
ctenidial retractor features do not allow postulation of con- 
specifity between Ch. montereyense and Ch. argenteum. A 
better knowledge of the geographical distribution of these 
two species (inshore and offshore regions) off British Co- 
lumbia, north to Vancouver, may shed more light on this 
matter. The nominal species Ch. attenuatum represents an 
“accident” or at least a mistake: since the sole sectioned 
specimen (= type) does not correspond to Heath’s own 
description and drawings, he obviously confused or mixed 
up series-sectioned material in the Hopkins Laboratory? 
and described a Ch. monereyense specimen as Ch. attenu- 
atum. 

Consequently, the synonymization of Chaetoderma at- 
tenuatum with Ch. montereyense (as could be suggested by 
Heath’s descriptions; see STORK, 1941:55), as well as of 
both these nominal species with Ch. argenteum (as done 
by SCHELTEMA et al., 1991) is rejected with respect to 
anatomical differences. The distinct specific validity of Ch. 
montereyense Heath is maintained along with Ch. argen- 
teum Heath; Ch. attenuatum Heath, however, is put into 
synonymy with Ch. argenteum. 


? The material described by Heath basically belonged to the 
MCZ at Harvard University (cf. HEATH 1911:9). The material 
to be elaborated (mainly serial sections) was taken by Heath to 
the Hopkins Laboratory, Stanford University, California. After 
Heath was dead, most of his collection was given by his son to 
the Hopkins Laboratory; other material was discarded (personal 
communication, K. Boss). Some slides were then taken by P. 
Riser from Hopkins Laboratory to Northeastern University, Na- 
hant, Massachusetts, and later forwarded to Harvard MCZ again 
(personal communication, K. Boss). In 1965, the slide material 


The Veliger, Vol. 36, No. 4 


at the Hopkins Laboratory was transferred to the California 
Academy of Sciences, from which STASEK (1966:1) listed the type 
specimens. 


LITERATURE CITED 


BUCKLAND-Nicks, J. & F.-S. CHIA. 1989. Spermiogenesis in 
Chaetoderma sp. (Aplacophora). Journal of Experimental 
Zoology 252:308-317. 

HEATH, H. 1911. Reports on the scientific results of the ex- 
pedition to the tropical Pacific ... XIV. The Solenogastres. 
Memoirs of the Museum of Comparative Zoology at Har- 
vard College 45(1):1-181. 

SALVINI-PLAWEN, L. v. 1972. Zur Morphologie und Phylo- 
genie der Mollusken. Zeitschrift fiir wissenschaftliche Zool- 
ogie 184:205-394. 

SALVINI-PLAWEN, L. v. 1975. Mollusca Caudofoveata. Marine 
Invertebrates of Scandinavia 4:1—-55. 

SALVINI-PLAWEN, L. v. 1978. The species-problem in Cau- 
dofoveata (Mollusca). Zoologischer Anzeiger 200:18-26. 

SALVINI-PLAWEN, L. v. 1985. Early evolution and the primitive 
groups. Pp. 59-150. In: E. R. Trueman & M. R. Clarke 
(eds.), The Mollusca 10 (Evolution). Academic Press: Or- 
lando, Florida. 

SALVINI-PLAWEN, L. v. 1988. The structure and function of 
molluscan digestive system. Pp. 301-379. In: E. R. Trueman 
& M. R. Clarke (eds.), The Mollusca 11 (Form and Func- 
tion). Academic Press: San Diego, California. 

SALVINI-PLAWEN, L. v. 1992. On certain Caudofoveata from 
the VEMA-Expedition. Proceedings of the Unitas Mala- 
cologica Edinburgh Congress 1986:317-333. E. Gittenber- 
ger & J. Goud, eds. 

SCHELTEMA, A. 1989. Australian aplacophoran molluscs: I. 
Chaetodermomorpha from Bass Strait and the continental 
slope off south-eastern Australia. Records of the Australian 
Museum 41:43-62. 

SCHELTEMA, A., J. BUCKLAND-Nicks & F.-SH. CHIA. 1991. 
Chaetoderma argenteum Heath, a northeastern Pacific apla- 
cophoran mollusk redescribed (Chaetodermomorpha: Chae- 
todermatidae). The Veliger 34:204-213. 

SCHWABL, M. 1963. Solenogaster Mollusks from southern Cal- 
ifornia. Pacific Science 17:261-281. 

STASEK, C. R. 1966. Harold Heath’s type Solenogasters (Mol- 
lusca, Amphineura, Aplacophora) in the California Acad- 
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casional Papers of the California Academy of Sciences 52: 
1-7. 

Stork, H. A. 1941. Solenogastren der Siboga-Expedition. Si- 
boga-Expeditie 47(b):48-70. 

WIREN, A. 1892. Studien tber die Solenogastres I. Monogra- 
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tenskaps-Akademiens Handlingar 24(12):1-66. 


The Veliger 36(4):413-424 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


An Empirical Evaluation of Various Techniques for 


Anesthetization and Tissue Fixation of Freshwater 


Unionoida (Mollusca: Bivalvia), with a Brief 


History of Experimentation in 


Molluscan Anesthetization 


by 


C. CLIFTON CONEY! 


Los Angeles County Museum of Natural History, 900 Exposition Boulevard, 
Los Angeles, California 90007, USA 


Abstract. 


The successful anesthetization and fixation of freshwater bivalves is necessary for study 


of their anatomy and fine structure. This need is further underscored by the possible elimination of 
many of the indigenous North American unionacean fauna by the introduced zebra mussel Dreissena 
polymorpha (Pallas, 1771). A number of techniques are empirically tested. The results of some of the 
various methodologies are compared using scanning electron microscopy. Optimal methods are suggested, 
with an additional primary treatment recommended for those genera that are difficult to anesthetize 
successfully. The literature on molluscan anesthetization methodology, exclusive of Cephalopoda, is 


reviewed. 


INTRODUCTION 


The preservation of the soft anatomy of mollusks is 
essential to taxonomists for correct systematic placement 
of the more problematic molluscan taxa. This is especially 
true in non-marine mollusks in which convergence of shell 
morphologies is exhibited in a number of rapidly evolving 
genera of the freshwater bivalve families Unionidae and 
Mycetopodidae. The need for careful preservation meth- 
odology of soft anatomy has been documented for the pres- 
ervation of land snails by EMBERTON (1989) and is further 
accentuated by the work of Davis et al. (1981), who dem- 
onstrated convergence in shell morphologies among ge- 
netically distinct species of the bivalve genus Elliptio. 

Students of the comparative anatomy of freshwater bi- 
valve unionid mollusks should anesthetize specimens to 
relax the tissues to their natural appearance, and follow 
up by proper tissue fixation with buffered glutaraldehyde 
in order to preserve lifelike anatomical specimens of fresh- 


' Published posthumously. Proofs read by Dr. James H. Mc- 
Lean. 


water bivalves. The techniques of anesthetization and tis- 
sue fixation recommended here are highly useful in the 
lifelike preservation of unionid bivalves for use in anatom- 
ical investigations of both gross comparative anatomy and 
for the exploration and documentation of microanatomy 
via scanning electron microscopy. Further tissue fixation 
using osmium tetroxide is required should anatomical 
analysis via transmission electron microscopy be desired. 
However, these techniques are not appropriate for molec- 
ular genetics studies requiring mitochondrial DNA ex- 
traction. 

There is some degree of urgency in adopting effective 
techniques. Since its introduction into the lower Great 
Lakes in 1985, the zebra mussel Dreissena polymorpha 
(Pallas, 1771) has spread rapidly and has been predicted 
to invade nearly all of the freshwater systems of North 
America (STRAYER, 1991). HUNTER & BAILEY (1992) pre- 
dicted that the effect of the zebra mussel upon freshwater 
unionids may possibly result in the virtual elimination of 
the indigenous North American unionid fauna. 

The history of experimentation with the anesthetization 
of various molluscan taxa, exclusive of the Cephalapoda, 


Page 414 


documents the use of a wide array of chemicals. Much of 
the previous experimentation on the anesthetization of 
mollusks has involved freshwater gastropods, largely as a 
result of parasitologically orientated research. Only one 
study has been undertaken to date on freshwater unionid 
bivalve taxa (FLORKIN, 1941). 

Finally, any person who intends to experiment with the 
chemical anesthesization of mollusks first must consult the 
appropriate MSDS chemical data sheets for precautionary 
safety and health recommendations, use a chemical fume 
hood and chemical fume safety masks, and wear appro- 
priate chemical hazard apparel. If experimentation in mol- 
luscan anesthetization with controlled substances such as 
sodium pentobarbital is desired, the investigator must ob- 
tain legal federal permits for such substances. The author 
is not responsible for any health problems of anyone who 
experiments with the substances and procedures described 
herein. 


MATERIALS anp METHODS 


Here I compare the anesthetic properties of nembutal, 
chloral hydrate, and 3-aminobenzoic acid ethyl ester, all 
followed by second stage treatment with 2-phenoxyethanol. 
I examine the results of killing of unionids in 70% ethanol, 
as well as 20% glutaraldehyde. I also compare the results 
of three anesthetization procedures in unfixed specimens 
that have been placed directly into 70% ethanol, with spec- 
imens that have been properly fixed with buffered glutar- 
aldehyde following anesthetization. Finally, I compare the 
results of fixation of specimens following anesthetization 
and placement directly into 70% ethanol. 

Specimens of two species of the genus Elliptio were 
collected by W. Henry McCullagh, from two localities on 
the St. Johns River system, Florida. Specimens were packed 
in ziplock plastic bags and shipped on synthetic ice over- 
night to the Los Angeles County Museum of Natural 
History (= LACM) where they were subjected to a variety 
of preservation methodologies. Elliptio icterina (Conrad, 
1834) s.l. [population described as Unio occulta (Lea, 1843) 
and subsequently synonymized under Elliptio icterina s.1. 
by JOHNSON (1970)] was collected in 0.5 to 1 m in depth 
from mud and detritus in Middle Haw Creek, a tributary 
of Crescent Lake, approximately 13 km southwest of Bun- 
nell, Flagler Co., Florida (29°23.2'N, 81°21.3’W), 18 July 
1992 (WHM 575 = LACM 92-49). Elliptio dariensis (Lea, 
1842) s.l. [population described as Unio monroensis (Lea, 
1843) and subsequently synonymized under Elliptio dar- 
zensis S.1. by JOHNSON (1970)] was collected in 1 m depth 
from a sandy mud substrate in the main stem of Black 
Creek at the public boat ramp at Middleberg, Clay Co., 
Florida (30°04.58'N, 81°50.58’W), 19 July 1992 (WHM 
577 = LACM 92-50). Additional specimens of Lampsilis 
sp. (possibly a new species; to be resolved in later systematic 
studies) were collected from the upper Alabama River 
system by Paul Hartfield, 25 June 1992 (PDH 92-32 = 
LACM 92-71.3). Lampsilis sp. were anesthetized and fixed 
via the primary methodology recommended herein and 


The Veliger, Vol. 36, No. 4 


subjected to intensive investigation of microanatomy via 
SEM. The results of that analysis are to be included in a 
broader paper dealing with the systematics of lampsilines; 
however, I document here the results of correct anesthe- 
tization and fixation procedure with respect to the cilia of 
the ctenidia, particularly the lifelike position of the later- 
ofrontal cilia. 

Davis et al. (1981) have shown that the Elliptio icterina 
group exhibits high genetic heterozygosity and numerous 
polymorphic loci, indicating that many of the 46 junior 
synonyms listed by JOHNSON (1970) deserve further study. 
Elliptio dariensis s.1. (Lea, 1842) is listed by JOHNSON 
(1972) as having only three junior synonyms. “Unio” mon- 
roensis (Lea, 1843) differs in shell morphology and type 
localities from Elliptio dariensis s.s. The Altamaha River 
is the type locality of E. darvensis s.s., whereas the St. Johns 
River system is the type locality of “Unio” monroensis. 
“Unio” occulta (Lea, 1843), and “Unio” monroensis (Lea, 
1843) may indeed be valid species of the genus Ellipto, 
and it may prove useful to document the anatomies of these 
two taxa for use by future systematists; however, it is not 
within the purview of this paper to present resolutions of 
taxonomic problems. 

Two primitive preservation methods, devoid of anes- 
thesia, were compared: two specimens (LACM 92-49.3) 
of Elliptio icterina s.1. [= Unio occulta] were pegged open 
and placed alive into 70% ethanol (see Table 1), and two 
additional specimens (LACM 92-49.4) were pegged open 
and placed alive into 20% glutaraldehyde (see Table 1). 
The use of formalin as a fixative was avoided, as even 
buffered formalin can destroy the chitinous rods of the 
demibranchs (personal observation) and render tissue hard, 
brittle, and useless for dissection within two to four years 
in land snails (SOLEM et al., 1981). 

Three primary, or first stage, anesthetics were used 
experimentally on specimens of both Elliptio icterina s.l. 
[= “Unio” occulta] and Elliptio dariensis s.l. [= “Unio” 
monroensis]: (1) 3-aminobenzoic acid ethyl ester (= tricaine 
methane sulfonate, = MS 222) at an initial concentration 
of 75 mg per liter of distilled water, followed by an ad- 
ditional 100 mg per liter of water every 6 hr, (2) unbuffered 
sodium pentobarbital (= nembutal) at an initial concen- 
tration of 100 mg per liter of distilled water, followed by 
an additional 50 mg liter of water every 6 hr, and (3) a 
single dose of 10 mg of chloral hydrate per liter of distilled 
water. Each anesthetic was used on an individual test 
group. Animals of both species were anesthetized with each 
treatment for 36 hr in distilled water. A second stage in 
the anesthetization process was the addition of 2-phen- 
oxyethanol administered at about 2 mL per animal with 
a pipette close to the incurrent apertures; this treatment 
followed all primary anesthetics for a duration of 12 hr. 
Specimens from each anesthetization treatment were then 
separated into two groups per species and per treatment. 
One group of specimens from each species and anesthetic 
treatment was placed directly into 70% ethanol without 
fixation, while the other group of specimens from each 
species and anesthetic treatment was taken from anesthetic 


C. C. Coney, 1993 


Table 1 


Page 415 


Comparison of results of various preservation methodologies in two species of Elliptio (Bivalvia: Unionidae). 


Branchial (incurrent) papillae of 


Treatmentf LACM E. 1. occulta LACM E. d. monroensis 
Killed in A 92-49.3* severe contraction not tested 

Killed in G 92-49.4* severe contraction not tested 

N-A 92-49.9 severe contraction 92-50.6* severe contraction 
CA 92-49.8 moderate contraction not tested 

TA not tested 92-50.5 moderate contraction 
N-A-G-A 92-49.9b moderate contraction not tested 
C-A-G-A 92-49. 8b* moderate contraction not tested 
T-A-G-A not tested not tested 
N-G--A 92-49.5 severe contraction 92-50.3* severe contraction 
C-G-HA 92-49.7* extended not tested 
T-G-A 92-49.6* fully extended 92-50.4* fully extended 


t Key to abbreviations of treatments: A = 70% ethyl alcohol; C = chloral hydrate; G = 20% glutaraldehyde; N = sodium pentobarbital 
(nembutal); T = 3-aminobenzoic acid ethyl ester (tricaine methane sulfonate). 


* Illustrated herein. 


and fixed in buffered 20% gluteraldehyde for 12 hr, rinsed 
in running tap water for 30 min, and then placed into 70% 
ethanol. 

Because of the extensibility of the branchial, or incur- 
rent, papillae in life, as well as their taxonomic value, I 
selected these tissues for study to determine the best anes- 
thetization and fixation methodology. Additionally, cten- 
idial ciliary structures of Lampsilis sp. (LACM 92-71.3) 
were investigated for the effects of anesthetization upon 
these structures. With the exceptions of LACM 92-49.8 
and LACM 92-49.9, which were adult males, all individ- 
uals selected for examination were adult females. For each 
specimen, the entire posterior mantle margin, inclusive of 
all branchial, or incurrent, papillae or ctenidia, was excised 
using small scissors under a dissecting microscope. These 
tissues were then placed into individual vials containing 
70% ethanol and labeled by species and treatment. Critical 
point drying of the tissues was accomplished by upgrading 
alcohol content from 70% to 95% to 100% ethanol, then 
transferring tissues to a mixture of 50% absolute ethanol 
and 50% hexamethyldisilizane, and finally to 100% hex- 
amethyldisilizane. Labeled tissues were placed in clean 
watch glasses and allowed to dry at room temperature 
under a chemical fume hood. Dried tissues were mounted 
on Cambridge S-4 SEM stubs, gold coated, and examined 
with a Cambridge 360 scanning electron microscope. All 


micrographs were taken at a consistent magnification of 
DOT. 


RESULTS 


The results of the various experimental methodologies 
employed in this study on the contraction or extension of 
the branchial, or incurrent, papillae are summarized in 
Table 1. 

As expected, the branchial papillae of two specimens of 
Elliptio icterina s.\. [= “Unio” occulta] that were pegged 


open and placed alive in 70% ethanol exhibited severe 
contraction (Figure 1). Severe contraction of the branchial 
papillae also occurred in two specimens of this same taxon 
that were pegged open and placed alive in 20% glutaral- 
dehyde (Figure 2). In both Elliptio icterina s.l. [= “Unio” 
occulta] and Elliptio dariensis s.1. [= “Unio” monroensis], 
moderate to severe contraction of the branchial papillae 
occurred when fully anesthetized specimens were placed 
in 70% ethanol without the benefit of fixation with glu- 
taraldehyde (Figure 3). Specimens of either species that 
had been previously anesthetized and preserved in 70% 
ethanol, and then fixed in glutaraldehyde, exhibited mod- 
erate, but not severe, contraction (Figure 4). Those treat- 
ments that involved an initial anesthetic, and a secondary 
introduction of 2-phenoxyethanol, followed by glutaral- 
dehyde fixation of fully anesthetized specimens, produced 
remarkably different results. The employment of unbuf- 
fered nembutal alone as the initial anesthetic resulted in 
severe contraction of the branchial papillae in both species 
tested (Figure 5); however, the foot of these animals ex- 
panded moderately, a response that would generally in- 
dicate that anesthetization was successful. On the other 
hand, the foot of those specimens treated with chloral hy- 
drate remained contracted and the valves of the shell simply 
gaped open upon anesthetization. However, the branchial 
papillae of two specimens so tested exhibited extension 
(Figure 6), thus indicating that anesthetization did occur. 
The methodology that produced the best and most consis- 
tent results was treatment with 3-aminobenzoic acid ethyl 
ester for 24 hr, followed by 2-phenoxyethanol for 12 hr, 
with fixation in 20% glutaraldehyde for 12 hr, followed 
by a 30 min continuous rinse in tap water, with final 
preservation in 70% ethanol. Both the foot and the bran- 
chial papillae of both species tested exhibited full and 
complete extension when subjected to 3-aminobenzoic acid 
ethyl ester as the initial anesthetic (Figures 7, 8). The 
laterofrontal cilia of the ascending lamella of the outer 


Explanation of Figures 1 to 4 


Figures 1-4. Comparison of branchial papillae resulting from various experimental preservation methodologies 
that have not benefited by fixation between relaxation and preservation in 70% ethanol. Figure 1. Elliptio icterina 
s.l. [= “Unio” occulta], LACM 92-49.3, showing severe contraction of papillae resulting from being pegged open 
and placed living into 70% ethanol. Scale bar = 1 mm. Figure 2. Elliptio icterina s.1. [= “Unio” occulta], LACM 
92-49.4, showing severe contraction of papillae resulting from being pegged open and placed living into 20% 
glutaraldehyde. Scale bar = 1 mm. Figure 3. Elliptio dariensis s.1. [= “Unio” monroensis], LACM 92-50.6, showing 
severe contraction following relaxation with nembutal and then preservation in 70% ethanol without the benefit of 
fixation in 20% glutaraldehyde. Scale bar = 1 mm. Figure 4. Elliptio icterina s.1. [= “Unio” occulta], LACM 92- 
49.9b, showing moderate contraction of papillae that have been relaxed with nembutal, preserved in 70% ethanol, 


The Veliger, Vol. 36, No. 4 


then fixed in glutaraldehyde and preserved again in 70% ethanol. Scale bar = 1 mm. 


demibranch of the ctenidia of Lampsilis sp. (LACM 92- 
71.3) that had undergone ideal anesthezation and fixation 
were found to be deployed in a lifelike configuration re- 
sembling a net, apparently so extended for the purpose of 
filtration (Figures 9-11). 

In recent experimentation, I have found that when 100 
mg of nembutal per liter of distilled water, buffered to a 
pH of 7.5 with Trizma HCI for tissue culture, is used as 
the initial anesthetic for 6 hr, followed by 3-aminobenzoic 
acid ethyl ester for 12 hr, and then by 2-phenoxyethanol 
for 12 hr, the amount of time needed to achieve full anes- 
thetization of specimens is reduced significantly, and full 
extension of foot and branchial papillae is obtained. Fur- 
ther experimentation with this three-stage process with 
nembutal as the primary anesthetic has resulted in suc- 


cessful anesthetization of both freshwater genera (e.g., Am- 
blema, Quadrula, and Uniomerus) and marine venerid gen- 
era (e.g., Mercenaria), all of which have been difficult to 
anesthetize satisfactorily. Additionally, for chemically sen- 
sitive unionaceans such as the lampsilines, excellent, life- 
like relaxation of tissues may be achieved by omitting the 
use of 3-aminobenzoic acid ethyl ester as an intermediate 
anesthetic and following through with continued additions 
of buffered nembutal at 100 mg per liter every 6 hr until 
the foot exhibits a significant decrease in tactile respon- 
siveness, at which time a few drops of 2-phenoxyethanol 
should be administered by pipette on the floor of the con- 
tainer near the incurrent aperture. Fixation with buffered 
20% glutaraldehyde buffered with collidine or sodium di- 
phosphate, following successful anesthetization by the above 


C. C. Coney, 1993 


Explanation of Figures 5 to 8 


Figures 5-8. Comparison of branchial papillae resulting from various experimental preservation methodologies 
that utilize fixation in glutaraldehyde between various relaxation techniques and final preservation in 70% ethanol. 
Figure 5. Elliptio dariensis s.l1. [= “Unio” monroensis], LACM 92-50.3, showing severe contraction of papillae 
resulting from relaxation with nembutal, followed by 2-phenoxyethanol, fixation in 20% glutaraldehyde, and 
preservation in 70% ethanol. Scale bar = 1 mm. Figure 6. Elliptio iceterina s.1. [= “Unio” occulta], LACM 92-49.7, 
showing partial extension of papillae resulting from relaxation with chloral hydrate, followed by 2-phenoxyethanol, 
fixation in 20% glutaraldehyde, and preservation in 70% ethanol. Scale bar = 1 mm. Figure 7. Elliptio icterina s.1. 
[= “Unio” occulta], LACM 92-49.6, showing full extension of branchial papillae resulting from relaxation with 
3-aminobenzoic acid ethyl ester, followed by 2-phenoxyethanol, fixation in 20% glutaraldehyde, and preservation 
in 70% ethanol. Scale bar = 1 mm. Figure 8. Elliptio dariensis s.l. [= “Unio” monroensis], LACM 92-50.4, showing 
full extension of branchial papillae resulting from relaxation with 3-aminobenzoic acid ethyl ester, followed by 


Page 417 


2-phenoxyethanol, fixation in 20% glutaraldehyde, and preservation in 70% ethanol. Scale bar = 1 mm. 


methodology, is mandatory for accurate lifelike anatomical 
preservation. 


DISCUSSION 


A review of the Materials and Methods sections of a 
surprisingly large number of papers reporting anatomical 
results for the purpose of justification of new species de- 
scriptions, or taxonomic revisions, within a wide diversity 
of mollusks (e.g., Unionidae, Pisiidae, Hydroiidae, etc.) 
revealed a failure to document any methodology employed 
in the anesthetization or fixation of molluscan tissues. A 
few of the more recent papers dealing with the comparative 


anatomy of members of the Unionoida that give no indi- 
cation of the anesthetization and fixation methodology used 
include MCMICHAEL & Hiscock (1958), PAIN & 
WOODWARD (1964), and SMITH (1979). 

A variety of anesthetization and fixation methodologies 
have been proposed for use on diverse molluscan taxa. 
FLORKIN (1941) is the only author to specifically address 
the problem of anesthetization of unionid bivalves. He 
evaluated the effects of four different barbiturates on An- 
donta and found nembutal to be the most effective of those 
tested. 

Morcu (1868) was apparently the first to recommend 
the addition of a chemical anesthetic (7.e., tobacco) in the 


The Veliger, Vol. 36, No. 4 


Explanation of Figures 9 to 11 


Figures 9-11. Ciliation of the ascending lamella of the outer demibranch of the ctenidia of Lampsilis sp. (LACM 
92-71.3) following anesthetization and fixation via the primary recommended methodology (see Text). Figure 9. 
General overview of the surface of the ascending lamella showing the arrangement of filaments and the location of 
Figure 10 as shown by rectangle outline. Scale bar = 200 um. Figure 10. Magnified portion from central area of 
Figure 9 showing a single ctenidial filament with reduced frontal cilia (F) and fully extended laterofrontal cilia 
(LF) in apparent natural position for filtering. Scale bar = 25 um. Figure 11. Highly magnified network of a single 
cluster of laterofrontal cilia showing the secondary microlaterofrontal cilia (SL) fully extended between the primary 
laterofrontal cilia fronds. Also seen are calcium phosphate concretions known to occur in the demibranchs of 


Unionaceans (see MCMAHON, 1991). Scale bar = 5 wm. 


preparation of mollusks for anatomical study, in this case 
pulmonate gastropods. A general review of methodologies 
is given below by technique. 


‘Techniques 


Freezing: GOHAR (1937) has recommended slowly 
freezing nudibranch gastropods, Paul Scott (personal com- 
munication, 1992) has successfully used freezing to relax 
a variety of marine gastropods, and A. H. Clarke (personal 
communication, 1991) observed that he had successfully 
relaxed freshwater unionids by slowly freezing them. 

Recently, I received an overnight shipment of live union- 
ids in which too much synthetic ice was used in layers 
above and below the plastic bags containing the bivalves. 
Upon opening the box, I found that all specimens were 
frozen. Although this was not a controlled experiment, it 
provided an unexpected opportunity to evaluate freezing 
as a method for relaxation of unionid bivalves. The results, 
however, were mixed, as different genera reacted in com- 
pletely different ways to freezing. Poor results were ex- 
hibited by various species of Elliptio, as the posterior man- 
tle margins had pulled away from the shell, curled inward, 
and contracted in death. Quite the opposite effect was 
observed in Villosa, as freezing produced some beautifully 
relaxed material in this genus. 


Cocaine: DALL (1892) recommended a 1% solution of 
cocaine, a legal substance at the turn of the twentieth 
century, for the anesthetization of mollusks in general. 
SIEBERT (1913) successfully used a 1% solution of cocaine 
to anesthetize Anodonta cellensis followed by fixation with 


Zenker’s solution and Flemming’s solution. However, 
SCHWANECKE (1913) reported that cocaine was unreliable 
for successful anesthetization of A. cellensis, and that an 
overnight exposure to a 3-4% solution of ammonium chlo- 
ride, followed by fixation with glacial acetic acid, produced 
the desired results in his study of the circulatory system 
of this species. As cocaine is a controlled substance, and 
therefore not readily available to most students of bivalve 
comparative anatomy, its usefulness as a bivalve anesthetic 
was not investigated here. 


Menthol: I have successfully employed menthol to anes- 
thetize aquatic pulmonate gastropods, and Paul Scott (per- 
sonal communication, 1992) has had successful results in 
using menthol to anesthetize marine bivalves of the family 
Cardiidae, but I have not found menthol to be effective in 
the anesthetization of unionids. ABDEL-MALEK (1951) re- 
ported menthol to be useful in the anesthetization of hel- 
minths, and menthol serves as one of the ingredients in 
more complex anesthetization formulas of McCRaw (1958) 
and of VAN EEDEN (1958); however, VAN DER SHALIE 
(1953) noted that menthol produced unpredictable results 
in pulmonates. GOHAR (1937) reported that tissue mac- 
eration occasionally occurred prior to anesthetization using 
menthol, and RUNHAM et al. (1965) reported that menthol 
used alone took a prolonged time to take effect, which may 
explain the maceration reported by GOHAR (1937). Suc- 
cessful anesthetization of hydrobiid gastropods using men- 
thol, followed by tissue fixation using either formalin or 
Bouin’s solution, was accomplished by THOMPSON (1968, 
1984) and by HERSHLER & THOMPSON (1992). 


C. C. Coney, 1993 


Magnesium chloride: LEIBOWITZ (1976) recommended 
the use of magnesium chloride as an initial anesthetic for 
marine gastropod veliger larvae, followed by propylene 
phenoxetol as a second stage anesthetic. STIRLING et al. 
(1984) used magnesium chloride as a primary stage an- 
esthetic, followed by benzocaine (ethyl-4-aminobenzoate) 
and procaine hydrochloride to anesthetize the veliger lar- 
vae of the marine pulmonate Amphibola crenata. RUNHAM 
et al. (1965) reported excellent anesthetization results for 
pulmonates by injecting them with a 10% solution of mag- 
nesium chloride. CHUNG (1985) reported that a solution 
consisting of 2% magnesium chloride and 0.01% succi- 
nylcholine chloride produced ideal results when injected 
into Helix aspersa Muller. AVELAR & SANTOS (1991) used 
magnesium chloride to relax Castalia undosa undosa of the 
freshwater bivalve family Hyriidae; however, I do not 
recommend magnesium chloride for unionids as I have 
observed unionids to react negatively—the introduction of 
a 1% solution caused contraction and death. 


Succinylcholine chloride: BEEMAN (1968) and Mart- 
ERA & Davis (1982) used an injection of succinylcholine 
chloride in a seawater solution to anesthetize nudibranch 
gastropods. BURTON (1975) anesthetized Helix pomatia by 
injecting individuals with succinylcholine chloride, and 
CHUNG (1985) used this in combination with magnesium 
chloride to anesthetize Helix aspersa. But I have not ex- 
plored the use of sucinylcholine chloride as an anesthetic 
for freshwater bivalves. 


Chloral hydrate: Chloral hydrate was recommended 
for the anesthetization of opistobranch gastropods by ARIAS 
et al. (1985). VAN EEDEN (1958) used a combination of 
menthol and chloral hydrate followed by immersion of 
extended pulmonates in boiling formalin; however, EM- 
BERTON (1989) reported that chloral hydrate was only 
partially successful as an anesthetic for pulmonates. The 
present study demonstrates that chloral hydrate is not an 
ideal anesthetic for unionid bivalves. 


2-phenoxyethanol: Propylene phenoxetol was used by 
OWEN (1955) to anesthetize marine bivalves; it also was 
used for marine and terrestrial gastropods (OWEN & 
STEEDMAN, 1958) with variable results. RUNHAM et al. 
(1965) used propylene phenoxetol in combination with 
nembutal to successfully anesthetize pulmonate slugs. Pro- 
pylene phenoxetol is no longer available from chemical 
supply houses in the United States; however, a related 
compound, 2-phenoxyethanol, is a satisfactory substitute, 
and its effect on the anesthetization of unionid bivalves is 
discussed in this study. 


3-aminobenzoic acid ethyl ester: This chemical, also 
known as tricaine methane sulfonate, methanesulfonate 
salt, and M.S. 222, was first reported to be highly suc- 
cessful in the anesthetization of cold blooded animals, in 
this case frogs, by ROTHLIN (1932). The chemical 
3-aminobenzoic acid ethyl ester has been used as a com- 
ponent of a variety of chemical treatments in the course 


Page 419 


of anesthetization of various aquatic pulmonates by JOOSSE 
& LEVER (1959), LEVER et al. (1964), LIEBSCH et al. (1978), 
and MutTani (1982). Attempts by Roland Anderson, Se- 
attle Aquarium (personal communication) to anesthetize 
Anodonta oregonensis and A. kennerly: using Finquel MS 
222 have failed to produce satisfactory results, and I sus- 
pect that this failure is due to an industrial defect in chem- 
ical purity, rather than other factors, as I have achieved 
excellent results using 3-aminobenzoic acid ethyl ester on 
A. kennerly: that were collected from the same locality and 
habitat as were those that Roland Anderson attempted to 
anesthetize. The results of anesthetization of unionids us- 
ing 3-aminobenzoic acid ethyl ester are documented in this 
study. 


Nembutal: I have found nembutal (= sodium pento- 
barbital) to produce excellent results in. pulmonates, and, 
if correctly buffered, to be an important primary stage 
anesthetic for freshwater unionids such as Amblema, Quad- 
rula, and Uniomerus, as well as marine venerid bivalves 
such as Mercenaria, all of which I have found to be difficult 
to anesthetize satisfactorily. WAN DER SHALIE (1953) rec- 
ommended a 10% solution of nembutal for the anestheti- 
zation of the terrestrial prosobranch gastropod Pomatiopsis. 
MEIER-BROOK (1976) reported excellent results for fresh- 
water pulmonates, prosobranchs, and Piszdium spp. using 
pentobarbital acid, advising that this is superior to nem- 
butal; however, HEARD (1965) employed a 10% solution 
of nembutal to successfully anesthetize a variety of Prsidium 
species. Nembutal has been reported to successfully anes- 
thetize a variety of Unionidae, including Fusconaia masoni 
(Conrad, 1834) as studied by FULLER (1973), as well as 
several species in the genus Lampsilis (KRAEMER, 1981; 
KaT, 1983). BARKER (1981) presented observations sup- 
porting the use of nembutal for the anesthetization of pul- 
monates. ZAWIEJA (1980) recommended the use of “Vet- 
butal,” or veterinary nembutal, for the anesthetization of 
Lymnaea stagnalis (Lymnaeidae). JOURDANE & THERON 
(1980) successfully anesthetized Biomphalaria glabrata 
(Planorbidae) using a 0.08% solution of nembutal. RUNHAM 
et al. (1965) reported excellent results from using a 0.08% 
solution of nembutal, followed by a 1% solution of pro- 
pylene phenoxetol, to anesthetize pulmonate slugs. Nem- 
butal has been used with other chemicals for the anesthe- 
tization of mollusks in a variety of combinations. MCCRAW 
(1958) used nembutal followed by the addition of menthol 
to anesthetize aquatic pulmonate gastropods, and KE- 
AWJAM (1986) reported that menthol followed by nembutal 
was useful in the anesthetization of Pila (Pilidae). JOOSSE 
& LEVER (1959) used nembutal followed by M.S. 222 (= 
tricaine methane sulfonate, = 3-aminobenzoic acid ethyl 
ester) to anesthetize Lymnaea; and LEVER et al. (1964) has 
combined nembutal and M.S. 222 with water that has 
been aerated with N, and CO, gases for the anesthetization 
of aquatic pulmonate gastropods. LIEBSCH ef al. (1978) 
modified the method of LEVER et al. (1964) by using a 
0.1% solution of nembutal aerated first with CO, gas, 


Page 420 


followed by aeration with N, gas to anesthetize specimens 
of Biomphalaria glabrata. MUTANI (1982) successfully used 
the method described by JOOSSE & LEVER (1959) to anes- 
thetize aquatic pulmonates; however, KEAWJAM (1986) 
found the method of JOOossE & LEVER (1959) to be un- 
satisfactory on specimens in the Pilidae. The effects of 
nembutal on unionids is discussed in this study. 


Other methodologies: A few other unusual method- 
ologies have been employed in the anesthetization of mol- 
lusks and are mentioned briefly here. CARRIKER & BLAKE 
(1959) utilized Sevin (1-naphthyl N-methyl-carbamate) 
followed by killing on dry ice to successfully anesthetize 
muricid gastropods, and HOFFMAN (1986) recommended 
the addition of acetone to Sevin, a rather insoluble com- 
pound, to act as an aid in dissolving this compound into 
seawater. BAILEY (1969) used carbon dioxide from dis- 
solving dry ice in water to anesthetize slugs. GREGG (1944) 
recommended simply drowning land slugs to relax them, 
and HuBRICHT (1951) recommended the addition of a 
saturated solution of Chloretone to the drowning process 
for land slugs. Chloretone was also used by CLEMENT & 
CATHER (1957) in the anesthetization of marine gastropod 
veliger larvae. PRINCE & FORD (1985) experimented with 
both diethyl carbonate and ethanol in the anesthetization 
of the marine abalone Haliotis ruber and found ethanol to 
be both safer and more effective than diethyl carbonate. 
DE WINTER (1985) used a 10% to 25% solution of ethanol 
to anesthetize and kill slugs. Amylocaine hydrochloride at 
1% (= Stovaine) has been used by SMITH (1961) on nu- 
dibranchs. Althesin, benzyl alcohol, ethanol, nembutal, and 
xylazine were all used experimentally by BOURNE (1984) 
to anesthetize the moon snail Polinices lewisi, with xylazine 
demonstrating the best results. Urethane (= ethyl carba- 
mate) has been used for anesthetization of aquatic pul- 
monate gastropods by MICHELSON (1958), ether for anes- 
thetization of terrestrial pulmonate gastropods by 
RIPPLINGER & JOLY (1960), and thin leaves of celluloid 
in photoxilinin ether for anesthetization of Anodonta by 
Kocu (1916). Successful anesthetization of Lymnaea stag- 
nalis (Lymnaeiidae) using halothane, enflurane, and iso- 
flurane was reported by GIRDLESTONE et al. (1989). 


RECOMMENDATIONS For FRESHWATER 
BIVALVES 


Complete immobility of the holding pans is necessary 
for the anesthetization treatments to be successful. This is 
best done in a controlled laboratory environment, rather 
than in the field. When in the field for extended periods 
of time, I have kept freshwater bivalves alive for a week 
while traveling in a hot car in the deep south of the United 
States by keeping the animals on ice in sturdy ice chests 
with a change of ice every 24 hr. Freshwater bivalves 
should be anesthetized with one of the following meth- 
odologies: (1) add 75 mg of 3-aminobenzoic acid ethyl ester 
per liter of distilled water initially, followed by an addi- 
tional 100 mg of 3-aminobenzoic acid ethyl ester at 60 hr 


The Veliger, Vol. 36, No. 4 


intervals for 24 to 120 hr, or until the foot exhibits little 
response to stimuli, followed by a few drops of 
2-phenoxyethanol introduced via pipette on the base of the 
container near the incurrent aperture for 12 to 24 hr, or 
(2) 100 mg of nembutal per liter of distilled water buffered 
to a pH of 7.5 with Trizma HCl for tissue cultures for 
the first 24 hr, followed by 100 mg per liter of 
3-aminobenzoic acid ethyl ester, followed by a few drops 
of 2-phenoxyethanol for 12 to 24 hr (a recommended pro- 
cedure for tenacious, thick-shelled bivalves such as Quad- 
rula), or (3) 100 mg of nembutal per liter of distilled water 
buffered to a pH of 7.5 with Trizma HCI for tissue culture 
for 48 to 72 hr, omitting the use of 3-aminobenzoic acid 
ethyl ester, followed by a few drops of 2-phenoxyethanol 
as response to stimuli fails (a recommended procedure for 
the more delicate lampsilines). 

After the species have acclimated to a holding pan of 
native or distilled water and have begun siphoning and 
moving about, 75 mg of 3-aminobenzoic acid ethyl ester 
per liter of distilled water should be lightly sprinkled over 
the surface of the water initially, followed by 100 mg of 
3-aminoenzoic acid ethyl ester per liter every 6 hr. One 
may determine when it is time to add the 2-phenoxyethanol 
by probing the extended foot. If a significantly reduced 
reaction to this stimulus is observed, then the specimen is 
ready for the addition of 2-phenoxyethanol. Using an eye- 
dropper, 2-phenoxyethanol should be introduced on the 
bottom of the holding pan close to the posterior siphons 
and the specimen should be allowed to continue anesthe- 
tization for another 12 hr. Some experimentation with 
quantities of anesthetics and time of treatment may be 
required to determine what combination works best for 
each genus. Care should be taken to separate genera into 
separate pans for anesthetization, as species in many gen- 
era anesthetize at very different rates. For example, Lamp- 
silis, Villosa, and other Lampsilini tend to anesthetize rath- 
er quickly (24 hr); Elliptio, Pleurobema, and other 
Pleurobemini take longer to show results; and such Am- 
blemini as Quadrula and Megalonaias may take up to 120 
hr to anesthetize, if buffered nembutal is not employed as 
the initial anesthetic. If genera are mixed in the holding 
pans, those that anesthetize earliest may begin to macerate 
and foul the water, causing those that would tend to anes- 
thetize later to retract and not anesthetize properly. 


pH: Proper control of pH is fundamental to both the 
anesthetization and the fixation of mollusks, and this is 
especially true for freshwater bivalves. TOWNSEND (1973) 
found that nembutal buffered with acetate to a slightly 
acidic pH (6.0) was helpful in the anesthetization of the 
planorbid snail Biomphalaria glabrata. Improved tech- 
niques for the successful anesthetization of Helisoma duryi 
(Planorbidae) by KUNIGELIS & SALEUDDIN (1984) using 
nembutal was enhanced by regulating increase in pH, 
caused by the ionization of nembutal, with Trizma buffer. 
In these two studies, buffers were used to extend the life 
of near neutral pH during anesthetization with barbitu- 


Ces Coney, 1993 


rates of a high pH, thus enhancing tissue penetration by 
the un-ionized anesthetic. Barbiturates have a high pH, 
and are used occasionally by chemists as buffering agents. 
Aldehydes, on the other hand, tend to have an acidic pH 
(3-6), and HoLt & Hicks (1961) have reported that bar- 
biturate buffers tend to react adversely with aldehydes. J. 
D. Williams (personal communication) found that fresh- 
water bivalves tend to contract into their shells when placed 
in an aldehyde fixative following complete anesthetization 
of the animals using unbuffered nembutal. KITIKOON & 
RIVERA (1982) found it highly useful to kill specimens of 
Tricula (Hydrobiidae) with Curarine following anesthe- 
tization with nembutal to keep the animals from retracting 
into their shells in response to glutaraldehyde fixation; 
however, they did not explore the reason behind this con- 
traction response. In this study, animals anesthetized with 
unbuffered nembutal and fixed with glutaraldehyde ex- 
hibited pronounced contraction of the branchial papillae 
(see Figures 3, 5). I suspect that this contraction is a 
physiological response to a marked difference in the pH 
of the anesthetic and that of the fixative. Maintenance of 
near neutral pH during nembutal anesthetization will not 
only enhance the penetration effect of the nembutal into 
the tissues, but may also be useful in controlling stimulus/ 
response reactions of anesthetized animals to pH changes 
resulting from the fixative, even though the fixative has 
been buffered to a neutral pH, because as the aldehyde 
polymerizes in the presence of a buffer (HayaT, 1981), 
pH undoubtedly fluctuates. 


Fixatives: ELLIS (1978) recommends the use of 70% 
industrial alcohol to preserve unionid specimens, and 
WOODWARD (1964, 1965, 1969) cites “spirit” (presumably 
ethyl alcohol) preserved specimens in his studies. Some 
authors (VEITENHEIMER & MANSUR, 1978; FULLER, 1972) 
have stated that tissue fixation has been accomplished using 
70% alcohol, or ethanol. Students of molluscan compara- 
tive anatomy should be wary of studies that state that tissue 
fixation was achieved using any type of alcohol. Alcohol 
is definitely not a tissue fixative; rather it dehydrates cells 
and tissues, thus causing pronounced tissue shrinkage and 
consequent morphological distortion. “The main objectives 
of fixation are to preserve the structure of cells with min- 
imum alteration from the living state with regard to vol- 
ume, morphology, and spatial relationships of organelles 
and macromolecules, minimum loss of tissue constituents, 
and protection of specimens against subsequent treatments 
including dehydration, embedding, staining, vacuum, and 
exposure to the electron beam” (HayArT, 1981). 

Aldehydes such as formaldehyde, acrolein, glutaralde- 
hyde, as well as other chemicals, particularly osmium te- 
troxide, have been used to fix tissues. For mollusks, the 
choice of an appropriate fixative is of critical importance. 
SOLEM et al. (1981) reported that land molluscan material 
that had been fixed in buffered formalin and subsequently 
transfered to alcohol became unusable in 2 to 4 years. 
Several studies have been based on unanesthetized speci- 


Page 421 


mens that had been initially fixed in 8-10% formalin and 
transfered to 70% ethanol, a practice recommended by 
Murray & LEONARD (1962) and MCMAHON (1991), and 
employed by CASTAGNOLO ef al. (1980), and MANSUR & 
SILVA (1990), or preservation in a mixture of formalin & 
alcohol (KILIAs, 1956). On the other hand, HAyaT (1981) 
noted that “no other fixative has surpassed glutaraldehyde 
in its ability to cross-link and preserve tissue proteins for 
routine electron microscopy.” I have used buffered glu- 
taraldehyde to fix anesthetized unionids with excellent re- 
sults, and tissues so fixed have remained in good condition 
for the past three years. A few studies of gill ciliation 
apparently have not found it necessary to employ anes- 
thesia in order to obtain results. Way et al. (1989) injected 
living unionids with a 2% solution of glutaraldehyde in 
0.1 M Sorenson’s phosphate buffer, and TTANKERSLEY & 
Dimock (1992) dissected living unionids and placed the 
ctenidia in a 2% solution of glutaraldehyde in 0.2 M So- 
renson’s phosphate buffer and post-fixed the tissues in a 
2% solution of cacodylate buffered osmium tetroxide. I 
have found that the laterofrontal cilia of the ascending 
lamella of the outer demibranch of the ctenidia of Lampsilis 
sp. (LACM 92-71.3) that have undergone ideal anesthe- 
zation and fixation are deployed in a lifelike configuration 
resembling a net, apparently so extended for the purpose 
of filtration (Figures 9-11). This observation of what is 
apparently the natural position of the laterofrontal cilia of 
the ctenidia differs significantly from the position of these 
cilia as described by workers who simultaneously killed 
the animals and fixed the tissues in buffered 2% glutar- 
aldehyde without the benefit of anesthesia (Way et al., 
1989). 

Hayat (1981) provided an excellent review of buffering 
chemicals for various fixative agents and their properties. 
Of those, I have found that sodium bicarbonate serves as 
a useful, inexpensive, and non-toxic buffer for tissue fix- 
ation using glutaraldehyde. Both TANKERSLEY & DIMOCK 
(1992) and Way et al. (1989) successfully used sodium 
diphosphate to buffer glutaraldehyde to a pH of 7.2 for 
fixation of unionids. HAYAT (1981) gave high marks to 
collidine as a buffer for glutaraldehyde, and I have found 
collidine to be a more efficient buffer than sodium bicar- 
bonate or sodium diphosphate. As any increase in pH 
above neutral accelerates polymerization and consequent 
deterioration of glutaraldehyde, a buffered stock solution 
has a limited shelf life. However, I have successfully re- 
used a buffered 20% solution of glutaraldehyde several 
times over before the solution exhibited noticeable poly- 
merization, as may be detected when the glutaraldehyde 
turns a dark yellow color. It is best to filter the fixative 
solution between uses to avoid contamination with glo- 
chidia from previous uses. Glutaraldehyde will deteriorate 
via polymerization with time, and this deterioration ac- 
celerates rapidly as a result of either a sharp rise in either 
temperature or pH. Deterioration of glutaraldehyde can 
be minimized by storing it as an unbuffered 25% solution 
at subfreezing temperatures (—20°C). Glutaraldehyde is 


Page 422 


a hazardous chemical and the use of rubber gloves and a 
chemical fume hood is imperative. Use of chemical fume 
mask and protective eye goggles are strongly recommended. 
Following fixation, the specimens should be rinsed under 
gently flowing tap water for about 30 min and then pre- 
served in 70% ethanol. If ethanol is not available, 50% 
isopropyl alcohol can be used as a temporary preservative. 
Permanent storage in isopropyl alcohol will harden the 
soft parts over time. Some workers prefer to add 1-3% 
glycerine to their alcohol-preserved specimens (Mc- 
MaAHon, 1991) so that the soft bodies will be kept moist 
should the alcohol evaporate over time; however, TURNER 
(1976) cautioned against the use of glycerol if specimens 
are to be examined using SEM analysis. I suspect that 
glycerol-treated specimens would result in undesirable 
coating of ciliary tracts or other fine surface structures of 
the anatomy, and also recommend against its use. 


SUMMARY 


Chemically induced anesthetization of freshwater mus- 
sels is of critical importance to the bivalve anatomist, as it 
allows the animal to be preserved in lifelike condition; 
however, unless such anesthetization is followed by tissue 
fixation in a suitable fixative, the results will be unsatis- 
factory. 

The anesthetic 3-aminobenzoic acid ethy] ester, followed 
with 2-phenoxyethanol, and fixation with glutaraldehyde, 
has been demonstrated here to produce reliably anesthe- 
tized anatomical specimens. A. Lopez has used this method 
in his laboratory in Managua, Nicaragua, with outstand- 
ing success on both Nicaraguan Mycetopodidae (Etheri- 
acea) and Unionidae. As noted above, much time may be 
saved, and some genera that are difficult to anesthetize 
may benefit substantially, by the use of buffered nembutal 
as the initial anesthetic if it is then followed by the pro- 
cedure recommended in this paper. Nembutal is the an- 
esthetic of choice for pulmonate gastropods, but produces 
unsatisfactory results when used alone and unbuffered on 
freshwater unionid bivalves. Use of chloral hydrate is not 
recommended. Although it produced moderate extension 
of the branchial papillae, the foot remained completely 
contracted and this condition would be counterproductive 
to any exploration of the coiling of the digestive tract within 
the foot. 

Without proper fixation, however, anesthetization ef- 
forts will fail, because anesthetized, or even apparently 
dead, specimens will undergo tissue contraction when placed 
directly into 70% ethanol. Tissue contraction will become 
severe when unfixed tissues are taken through a graded 
alcohol series to absolute alcohol and then into hexame- 
thyldisilizane to obtain critically dried tissues for SEM 
analysis. A freshly buffered 20% solution of glutaraldehyde 
is the preferred fixative, and 12 hr an ideal fixation time. 


ACKNOWLEDGMENTS 


I express my sincere appreciation to W. Henry Mc- 
Cullagh, M.D. of Jacksonville, Florida, for numerous col- 


The Veliger, Vol. 36, No. 4 


lections of living unionids, all documented with meticulous 
field notes, and for the additional effort of overnight ship- 
ping of numerous living specimens. Alan L. Mosley, M.D. 
and Kenneth Hemkin, Pharm. D. graciously provided 
nembutal for experimental anesthetization of subject ma- 
terial. Dr. Al Lopez, S.J., Universidad de Centro Amer- 
icana, Managua, Nicaragua, was instrumental in dem- 
onstrating that the methodology described in this paper 
could be used successfully in a tropical environment on 
various genera of the Mycetopodidae. Drs. Henry Chaney, 
Santa Barabara Museum of Natural History, and Silvard 
P. Kool, Museum of Comparative Zoology, kindly pro- 
vided assistance with some of the rare literature. Helga 
Schwarz, Ichthyology Section, LACM, graciously trans- 
lated several German texts. Jennifer Edwards, Research 
Library, LACM, was very helpful in obtaining needed 
literature through interlibrary loan. Donald McNamee, 
Chief Librarian, Research Library, LACM, provided a 
computer search of literature on anesthesia of Mollusca 
published since 1968. Dr. Anthony R. Kampf, Curator of 
Minerals & Gems, LACM, kindly provided access to, and 
assistance with, a precision balance for quantification of 
chemicals used in molluscan anesthesia. Appreciation is 
also expressed to Alicia Thompson and Jack Worrall of 
the University of Southern California for their advice with 
SEM operation. SEM negatives were printed by John De 
Leon, Photography Section, LACM. Suggestions by Drs. 
Arthur E. Bogan and Eugene V. Coan are also appreci- 
ated. Useful information was contributed to this study by 
Arthur H. Clarke, Paul H. Scott, and James D. Williams. 
Dr. James H. McLean, Lindsey T. Groves, Gary A. Pettit 
(all of LACM), Paul D. Hartfield of the U.S. Fish and 
Wildlife Service, Jackson, Mississippi, James D. Williams 
and Jayne Brim Box of the U.S. Fish and Wildlife Service, 
Tallahassee, Florida, M. Christopher Barnhart, South- 
western Missouri State University, and Paul H. Scott of 
the Santa Barbara Museum of Natural History reviewed 
the manuscript and offered helpful suggestions. This re- 
search was funded in part by the LACM Malacology Fund 
administered by Dr. James H. McLean, and in part by 
U.S. Fish and Wildlife Service grant number 14-16-0004- 
92-981 administered by Dr. Paul Hartfield, U.S. Fish and 
Wildlife Service, Jackson, Mississippi. 


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The Veliger 36(4):425-432 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


NOTES, INFORMATION & NEWS 


Effects of Restricted Food Intake on 
Hemolymph Glucose Concentration and 
Digestive Gland-Gonad Lipid Level in the 
Schistosome Vector Biomphalaria glabrata 
(Say) (Gastropoda: Planorbidae) 
by 
S. N. Thompson and V. Mejia-Scales 
Department of Entomology, 
University of California, 
Riverside, California 92521, USA 


Introduction 


The effects of starvation on storage metabolite levels have 
been examined in several mollusks. HEEG (1977), for ex- 
ample, demonstrated that lipid and carbohydrate reserves 
were reduced in the digestive gland and gonad of starved 
Bulinus africanus (Krauss). Similar depletion of lipid and 
carbohydrate reserves was reported in starved Biomphal- 
aria glabrata by DUNCAN et al. (1987) and CHRISTIE e¢ al. 
(1974), respectively. Moreover, several studies indicate that 
starvation was partially responsible for depletion of met- 
abolic reserves in schistosome-infected snails. Hemolymph 
glucose and glycogen reserves in the digestive gland were 
reduced in Biomphalaria glabrata infected with Schistosoma 
mansoni Sambon, and these effects were similar to those 
observed during starvation of normal uninfected snails 
(CHRISTIE et al., 1974; STANISLAWSKI & BECKER, 1979). 
On the basis of these and other observations, BECKER (1980) 
concluded that the parasite exerts profound effects on host 
metabolism by competing with host tissues for nutrients, 
thus inducing a state of starvation. Such nutritional com- 
petition, however, would not result in starvation per se, 
but rather, would reduce the availability of assimilated 
nutrients for snail tissues. Previous investigation has dem- 
onstrated that food consumption and assimilation were 
unaffected by infection, but snail conversion efficiency was 
significantly reduced in infected individuals (THOMPSON 
& MEJIA-SCALES, 1989). Because maturation and cercarial 
shedding of S. mansoni occur in a continuous daily cycle 
(JOURDANE & THERON, 1987), nutritional stress caused 
by infection may follow a similar diurnal rhythm. 

In contrast to the effects of schistosome infection on 
carbohydrate reserves, recent studies demonstrated that 
infection by Schistosoma mansoni caused an increased de- 
position of lipids in the digestive gland and gonad of Bzom- 
phalaria glabrata, supporting earlier histological observa- 
tions by others on a variety of trematode-infected mollusks 
(PORTER, 1970). Previous studies with other metazoan 
invertebrates including some flatworms demonstrated de- 
creased storage of carbohydrates, but accumulation of lipid 
during starvation (DAvIs & FRIED, 1977). CALLOW & 


JENNINGS (1974) reported that lipid was utilized by triclad 
turbellarians during starvation, but lipid synthesis and 
deposition were increased in response to decreased or re- 
stricted food intake. Subsequently, CALLOW & JENNINGS 
(1977) suggested that many free-living metazoans that face 
unpredictable but likely periods of food shortage may have 
developed optimal metabolic strategies for accumulating 
sufficient storage reserves beforehand to survive during 
starvation. They demonstrated that maximum food storage 
in the flatworm Dugesia lugubris (Schmidt) did not cor- 
respond to maximum food availability, but to a submax- 
imal level that signaled an impending period of food short- 
age. When animals were starved, their storage lipids 
decreased, but when pulse fed, that is, fed once/week, 
animals stored more lipid than individuals fed daily or 
every other day. 

We hypothesize, based on the conclusion by BECKER 
(1980), that the increased lipid level in infected Biom- 
phalaria glabrata may reflect a similar response to food 
shortage as that described above by CALLOW & JENNINGS 
(1977), in the case of B. glabrata, brought about by nutrient 
competition between the host and parasite. In the present 
study we attempted to mimic the effects of schistosome 
infection on hemolymph glucose and lipid levels in the 
digestive gland-gonad (DGG) by placing uninfected snails 
on a daily or weekly feeding regime. The effects of re- 
stricted food intake on storage metabolite levels in B. gla- 
brata have not been previously examined. 


Materials and Methods 


Stock colonies of Biomphalaria glabrata (albino M line 
strain) were reared and maintained in the laboratory on 
fresh Romaine lettuce supplemented with Tetramin® fish 
food as described previously (THOMPSON, 1987). For feed- 
ing trials, three 2-gallon (7.5-L) bottomless aquaria each 
containing 45 snails were submerged in a single 15-gallon 
(57-L) aquarium. The smaller aquaria rested on a plastic 
grid (1 cm? sections) supported approximately 2 cm from 
the bottom of the larger aquarium. Fecal material accu- 
mulated under the grid and was inaccessible to the snails, 
which otherwise exhibit coprophagy. Snails were main- 
tained in a commercial spring water (Arrowhead, Colton, 
California 92324) at room temperature, approximately 
26°C, under a 16:8 hr light/dark photoperiod. The aquaria 
were cleaned and filled with fresh spring water each week. 

Snails were treated in one of three ways: (1) fed whole 
lettuce ad libitum, (2) fed lettuce ad libitum once/week for 
24 hr, or (3) fed daily with a reduced portion of lettuce 
comprised of a single 5-cm? section of leaf randomly torn 
into several smaller pieces, which were totally consumed 
within 2 to 4 hr. Experiments were conducted for four 


Page 426 


The Veliger, Vol. 36, No. 4 


Table 1 


Effect of nutrient-deprivation on body and DGG (digestive gland-gonad complex) weight, lipid level, and hemolymph 
glucose concentration of Biomphalaria glabrata. 


Fresh weight (mg) 


Nutritional % 
treatment survival Total body DGG 
Replicate 1* 
ad libitum 96 0am ay SOS Aa 
fed daily 80 150 + 5* 42 + 2* 
fed 1/wk 60 135 + 6fF 40 + 2+ 
Replicate 2° 
ad libitum 70 AN 7/8) Oh BS) ee sh 
fed daily 50 IBS Asis 
fed 1/wk 32 1:12: EN 6* 32D 
Replicate 3* 
ad libitum 70 202 + 11* 64 + 4* 
fed daily 40 166: 32 112* 47 + 4* 
fed 1/wk 34 WAY a oh 2i6) ar oh 
Replicate 4* 
ad libitum 80 ND 89 + 5*F 
fed daily 62 ND Gis) as oe 
fed 1/wk 42 ND 47 + 4t 


52-5 b 
Mean lipid content Hemolymph 


ug/DGG mg/g DGG glucose (mg%) 
1112 12.8 Shi) ss OA 
431 10.4 4.6 + 0.2* 
368 9.0 6.3 + 0.4* 
645 11.8 3.4+ 0.1 
380 9.3 BY) ae (0),3} 
264 8.4 4.3 + 0.6 
732 11.2 4.6 + 0.4 
508 10.7 Bil se 05) 
327 10.0 6.4 + 0.9 
1159 13.1 4.4 + 0.4* 
529 9.1 3.3 + 0.8F 
428 9.2 8.1 + 0.7*F 


«x + SE, n = <43 based on survival; numbers in columns followed by the same symbol are significantly different statistically at the 


5% level as determined by Duncan’s multiple range test. 
» Based on pooled sample. 
ND = not determined. 


weeks, a time period consistent with the beginning of pa- 
tency in snails infected with Schistosoma mansoni. The he- 
molymph from individual snails was collected in capillary 
tubes by puncturing the heart through the shell. Snails 
were then gently crushed between two petri plates, the 
shell fragments carefully removed, and total body wet weight 
determined. The DGG was then dissected and weighed. 

The total lipid of the DGG from each group was ex- 
tracted from the pooled tissue in chloroform-methanol (1:2 
v/v) by the method of BLIGH & DYER (1959). The quantity 
of the final washed lipid was determined gravimetrically. 
Hemolymph was deproteinized with ZnSO,-Ba(OH), and 
the glucose concentration determined by the oxidase-per- 
oxidase method using a Sigma Diagnostics kit (Sigma 
Chemical Co., St. Louis, Missouri 63178). Standard glu- 
cose curves prepared with water or hemolymph gave the 
same results. 

Statistical analysis of data was performed by ANOVA 
followed by comparison of means using Duncan’s multiple 
range test. 


Results 


The results of feeding experiments with Biomphalaria gla- 
brata were highly variable. Data, therefore, are presented 
in replicate form (Table 1). In all cases, body and DGG 
fresh weight were reduced in nutrient-deprived snails. The 
proportion of body weight represented by the DGG, how- 
ever, was constant in all groups at 29.1 + 1.7% for all 


treatments in replicates 1 through 3. Snail mortality con- 
sistently increased with severity of food restriction. 

The mean lipid content per individual DGG, as well 
as in relation to the weight of DGG, was lower in the 
nutrient-deprived snails compared with controls fed ad 
libitum (Table 1). Snails fed once/week had lower lipid 
levels than those that underwent daily but restricted feed- 
ing. 

The hemolymph glucose of snails generally was elevated 
by nutrient deprivation and the results were diametrically 
opposite to those on lipid concentration (Table 1). That 
is, nutrient-deprived snails fed once/week had higher he- 
molymph glucose than those fed reduced rations daily. In 
most cases, however, glucose concentrations in the latter 
were not significantly different from those of snails fed ad 
libitum. 


Discussion 


During the present study, hemolymph glucose in Biom- 
phalaria glabrata was maintained or increased by restricted 
food intake (Table 1). THOMPSON & LEE (1986) failed to 
observe any difference in hemolymph glucose between 
starved B. glabrata and snails fed ad libitum, although other 
studies demonstrated decreased hemolymph glucose in 
starved snails (STANISLAWSKY & BECKER, 1979). Our re- 
sults with B. glabrata were similar to those of VELDHUIJZEN 
(1975) with Lymnaea stagnalis (Linnaeus). Starvation failed 
to cause a depletion of hemolymph glucose in that species. 


Notes, Information & News 


Moreover, a sharp rise in hemolymph glucose, similar to 
that observed during the present result with B. glabrata 
fed once/week, occurred in L. stagnalis when snails were 
fed following two weeks starvation. Hemolymph glucose 
was likely maintained at the expense of storage glycogen 
(CHRISTIE et al., 1974), or trehalose (ANDERTON ef al., 
1993) and hemolymph glucose level may provide a valuable 
indicator of this mobilization process in food-deprived snails. 

The present results on hemolymph glucose levels in 
Biomphalaria glabrata whose food intake was restricted are 
in marked contrast to results of studies with infected snails. 
Investigations to date have consistently demonstrated de- 
creased glucose levels in schistosome infected snails. This 
difference between infected and nutrient-deprived individ- 
uals may reflect differences in metabolic rates. Others have 
reported that respiration (7.e., oxygen consumption) in B. 
glabrata was unaffected or was increased during infection, 
and the increase in oxygen consumption was the result of 
respiration of snail tissues and not due to parasite metab- 
olism (LEE & CHENG, 1971; BECKER, 1980). In contrast, 
investigations with starved snails indicate that starvation 
causes a decrease in metabolic rate (WILLIAMS & GIL- 
BERTSON, 1983). Thus, mobilization of carbohydrate re- 
serves may occur similarly during infection and food de- 
privation, but glucose level in snails deprived of food may 
be unaffected or increased because the snail’s metabolic 
rate is reduced. 

Storage lipids in Biomphalaria glabrata were depleted in 
a similar manner by restricted food intake as reported by 
DUNCAN et al. (1987) in starved snails. It appears, there- 
fore, that the increased lipid previously observed in schis- 
tosome-infected individuals did not result from a parasite- 
induced food deprivation, in the manner hypothesized above. 
The role of lipid as a storage reserve in B. glabrata as well 
as other pulmonate gastropods is not clear. Although tri- 
glyceride may decrease during starvation in some species, 
glycogen appears to be the main storage metabolite utilized 
(CHRISTIE et al., 1974; HEEG, 1977; VELDHUIJZEN, 1975). 
MEYER et al. (1986) failed to observe increased ketone 
body formation in starved B. glabrata, further indicating 
that lipid may not be an important energy reserve. Thus, 
the role of lipids in the metabolism of snails and the po- 
tential significance of lipids to developing schistosomes re- 
quires further investigation. 


Literature Cited 


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BECKER, W. 1980. Metabolic interrelationship of parasitic 
trematodes and molluscs, especially Schistosoma mansoni in 
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Page 427 


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Duncan, M., B. FRIED & J. SHERMA. 1987. Lipids in fed and 
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HEEG, J. 1977. Oxygen consumption and the use of metabolic 
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JOURDANE, J. & A. THERON. 1987. Larval development: eggs 
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STANISLAWSKY, E. & W. BECKER. 1979. Influences of semi- 
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glabrata (Gastropoda). Comparative Biochemistry and Phys- 
iology 63A:527-533. 

THompson, S. N. 1987. Effect of Schistosoma mansoni on the 
gross lipid composition of its vector Biomphalaria glabrata. 
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Page 428 


Aggressive Behavior of the Whelk 
Morula musiva 
by 
Naoya Abe 
Intercultural Relations Department, 
Osaka International College for Women, 
6-21-57 Tohdacho, 
Moriguchi, Osaka 570, Japan 


Introduction 


Invasion of one animal’s resources by another individual 
often triggers an aggressive behavior. Among prosobranchs 
some limpets show aggressive behaviors (STIMSON, 1970; 
BRANCH, 1979, 1981; IWASAKI, 1992). However, in other 
prosobranchs aggressive behaviors have not been reported 
except for the fighting conch Strombus pugilis. In the lab- 
oratory males of this species fight for their mates using the 
proboscis (BRADSHAW-HAWKINS & SANDER, 1981). I found 
in the laboratory that Morula musiva (Kiener), a common 
whelk in the intertidal rocky shore of southwestern Japan, 
attacks conspecifics with the proboscis. In this report I 
describe the aggressive behavior of M. musiva and discuss 
the role of this behavior. 


Materials and Methods 


Individuals of Morula musiva were collected from the rocky 
shore of Shirahama, Japan (33°43'’N, 135°21’E) on 28 
April 1991, when the male mounting on the shell of the 
female was often encountered. Twenty-one mounting pairs 
were collected and each whelk was marked with an oil 
marker to distinguish the sex. Collected whelks were placed 
in an aquarium of 35 x 25 x 25 cm. The seawater was 
aerated and filtered. Some fresh water, less than ca. 4, of 
the water remaining, was occasionally added to keep the 
salt concentration constant. Whelks were fed living mussels 
(Septifer virgatus). Behaviors of whelks were observed five 
times a week from 8 May to 26 July 1991 (67 times in 
total). 

Supplemental laboratory observations were made on 17 
and 18 July 1992. In these observations a male was put 
near a mounting pair and behaviors were recorded with 
a video camera. 

Field observations were made on the rocky shore of 
Shirahama on 2-3 July 1993, where Morula musiva was 
abundant (ca. 12/m?) in tidepools dominated by the mussel 
Hormoya mutabilis. Behaviors of whelks in tidepools were 
observed for 5 hr during the daytime low tide and for 2 
hr during the nighttime low tide. 


Results 


Aggressive behaviors of Morula musiva were observed on 
15 occasions in 1991. On 13 occasions, attacks occurred 
between a mounting male and another male approaching 
the mounting pair. First, the mounting male lifted the 


The Veliger, Vol. 36, No. 4 


anterior part of his shell and then elongated his proboscis 
to seek the rival. These behaviors were induced by the 
direct contact of the rival with the soft body. The mounting 
male pressed the tip of proboscis against the rival’s body 
(Figure 1A). The attacked rival usually retracted his body 
instantly. Although on one occasion the rival quickly went 
down from the female’s shell, in the other cases he coun- 
terattacked the mounting male with his proboscis. When 
both of them elongated the proboscis, they often pushed 
each other with their proboscides (Figure 1B): repeatedly, 
one pushed and then the other pushed back. The fights 
usually terminated when one male dismounted the female’s 
shell, or occasionally, when one male dropped off (Figure 
1C, D). The duration of three fights, recorded from onset 
to termination, was 12, 32, and 48 min. 

Of 13 bouts, the mounting male recorded 11 wins, one 
defeat, and one unknown conclusion. Outcome was not 
related to the size of males: larger ones won three times, 
smaller ones six times, and sizes were similar between 
contestants (size difference <2 mm in shell length) in the 
other three cases. 

In addition to encounters between mounting and rival 
males, on two occasions aggressive behaviors were observed 
when a whelk feeding on a mussel was approached by 
another whelk. The contestants were heterosexual in one 
case, and homosexual in the other. In both cases they 
attacked each other in the same manner as when fighting 
over a mate, and in both cases the original occupant of the 
mussel won. 

Aggressive behaviors were observed twice in the field. 
In one case, the mounting male was attacked by another 
male with the proboscis, and dismounted the female’s shell 
without counterattacking. In the second case, two males 
attacked each other with their proboscides on the shell of 
a female. 


Discussion 


Aggressive behaviors of Morula musiva were observed in 
the laboratory and in the field. 

Attacking with the proboscis seems to be effective, be- 
cause the attached whelk retracted his body and occasion- 
ally dropped off the female’s shell (Figure 1C, D). The 
radula may have the ability to damage the body of a rival. 
The whelks elongated and curved the proboscis, the only 
apparatus the snail can manipulate like an appendage, 
smoothly to seek the rival. We can easily imagine the 
divergent usage of the proboscis as a weapon. 

Aggressive behaviors mainly occurred when a mounting 
male was approached by another male. In this conflict 
between males over a mate, mounting males won most 
contests even though their rivals usually counterattacked. 

Aggressive behaviors also occurred when a whelk feed- 
ing on Septifer virgatus was approached by another indi- 
vidual, although the frequency was low. This whelk al- 
ways drills a hole on the prey shell before feeding, and 


Notes, Information & News Page 429 


Figure 1 


Aggressive behavior of Morula musiva. A. A male (lower) mounting a female (middle) and being attacked by the 
proboscis of a rival male (upper). B. Males pushing each other with the proboscides. C, D. The fight resulted in 
the drop of the rival male from the female’s shell. 


drilling takes several hours to three days (ABE, 1989). aquarium may cause temporal robbery. In tidepools, scav- 
Thus, the drilled prey is of great value to both the original enging muricids Ergalatax contractus and Cronia margari- 
occupant and a robber. In the field, however, whelks feed ticola often gather around the mussel Hormomya mutabilis 


only on living animals (ABE, 1980). High density in the drilled by Morula musiva (Abe, unpublished data). Perhaps 


Page 430 


the aggressive behavior is important in guarding prey from 
such scavenging gastropods. 


Acknowledgments 


I thank K. Wada of Nara Women’s University for critically 
reading the manuscript. This work is supported by the 
Research Institute of Marine Invertebrates and forms a 
part of guest scientist activities, Center for Ecological Re- 
search, Kyoto University. 


Literature Cited 


ABE, N. 1980. Food and feeding habit of some carnivorous 
gastropods (preliminary report). Benthos Research 19/20: 
39-47 (in Japanese). 


The Veliger, Vol. 36, No. 4 


ABE, N. 1989. Prey value to the carnivorous gastropods Morula 
musa (Kiener) and the two forms of Thavs clavigera (Kus- 
ter): effect of foraging duration and abandonment of prey. 
Malacologia 30:373-395. 

BRADSHAW-HAWKINS, V. I. & F. SANDER. 1981. Notes on the 
reproductive biology and behavior of the West Indian fight- 
ing Conch, Strombus pugilis Linneaus in Barbados, with 
evidence of male guarding. The Veliger 24:159-164. 

BRANCH, G. M. 1979. Aggression by limpets against inverte- 
brate predators. Animal Behaviour 27:408-410. 

BRANCH, G. M. 1981. The biology of limpets: physical factors, 
energy flow, and ecological interactions. Oceanography and 
Marine Biology Annual Review 19:235-280. 

IwasaKI, K. 1992. Factors affecting individual variation in 
resting site fidelity in the patellid limpet, Cellana toreuma 
(Reeve). Ecological Research 7:305-331. 

Stimson, J. 1970. Territorial behaviour of the owl limpet, 
Lottia gigantea. Ecology 51:113-118. 


d 


Figure 1 


a and b are sides of the Nautilus pompilius specimen showing the position of the second band pattern, c shows the 
second band pattern on the dorsal side of the venter, and d shows the aperture of the shell. 


Notes, Information & News 


Band Color Pattern on the Venter of a Mature 
Shell of Nautilus pompilius Linnaeus, 1758 
by 
Kent D. Trego 
3895 LaSelva Dr., 

Palo Alto, California 94306, USA 


Recently a large shell of the cephalopod species Nautilus 
pompilius Linnaeus, 1758, was obtained with an unusual 
color pattern. The shell, reportedly from Indonesia, has a 
diameter of 195 mm, which implies mature size. 

Normally, the band color pattern is seen on approxi- 
mately the first one-third of the mature shell of any species 
of living Nautilus. On this particular specimen of N. pom- 
pilus, the band color pattern reappears on the white ventral 
area of the shell (Figure la-c). Appearance of the band 
color pattern on the venter of the mature shell of any species 
of living Nautilus species has never been reported. 

There are ten characteristics of the mature Nautilus shell 
(COLLINS & WARD, 1987). Eight of these ten character- 
istics are detectable through a simple inspection of the shell. 
Those eight characteristics listed in order of formation by 
COLLINS & WARD (1987) are: 


. Cessation of secretion of color bands on the shell. 
. Rounded broadening of the aperture. 

. Change in coiling. 

Contraction of the aperture. 

Deepening of the ocular sinuses. 

. Full growth of the mature body chamber. 

. Thickening of the apertural edge. 

. Secretion of the black band inside the aperture. 


CNYDAUAWNHH 


The specimen of Nautilus pompilius discussed here has 
all eight characteristics of shell maturity. (An apertural 
view of the shell is shown in Figure 1d.) Reasons for the 
resecretion of the band color pattern in this shell are not 
clear. 


Literature Cited 


Couns, D. & P. D. Warp. 1987. Adolescent growth and 
maturity in Nautilus. Pp. 421-432. In: W. B. Saunders & 
N. H. Landman (eds.), Nautilus the Biology and Paleobiol- 
ogy of a Living Fossil. Plenum Press: New York. 


Range Extension for the Land Snail 
Eremarionta rowelli hutsoni 
(G. H. Clapp, 1907) 
by 
James E. Hoffman 
HCR1 Box 1536P, 
Tucson, Arizona 85736, USA 


On 24 March 1992, while performing field research for a 
status survey sponsored by the U.S. Fish and Wildlife 
Service, I found two live adult and several shells of Evre- 


Page 431 


marionta rowelli hutsoni (G. H. Clapp, 1907) in the north 
end of the Sierra Estrella in Maricopa Co., just southwest 
of Phoenix, Arizona. These snails were found in rocks 
lining a north-facing ravine at 112°20.4’W, 33°20.8'N, at 
an elevation of 393 m. This locality is approximately 187 
km east of the nearest previously known locality for Er- 
emarionta Pilsbry, 1913. The nearest previously known 
locality is the type locality for E. r. hutsoni and is located 
in the northern foothills of the Dome Rock Mountains at 
ca. 114°20’W, 33°35’N, about 6 km west of the town of 
Quartzsite. 

Of the subspecies of Eremarionta rowelli, the snails from 
the Sierra Estrella resemble E. r. hutsonz in every important 
way. PILSBRY (1939) describes EF. r. hutsoni as being dis- 
cernible from other subspecies of Eremarionta rowelli (W. 
Newcomb, 1865) by virtue of a broad brown band on the 
top of its shell. This broad band is separated from the dark 
brown peripheral band common to Eremarionta by a thin 
white line. The broad brown band extends to the suture, 
is lighter in color than the peripheral band, and is most 
obvious when viewed on the inside through the aperture. 
Below the dark band the shells are light cream colored. 

The shells I collected are typical Evemanionta rowelli 
hutsoni. The three adult shells all consisted of 4% whorls, 
their height varied from 8.7 to 9.2 mm, their greatest 
diameter from 14.5 to 15.5 mm, their peristome height 
from 7.1 to 7.6 mm, and each shell collected had papillose 
embryonic whorls common to Evemarionta (PILSBRY, 1939). 

The reproductive tracts of the two snails that I was able 
to dissect have typical Evemarionta characteristics as enu- 
merated by BEQUAERT & MILLER (1973). These include 
a dart sac seated on the vagina with two membranous 
mucous glands attached near its base, and a prominent 
diverticulum on the spermathecal duct. 

The finding of Eremarionta in the Phoenix area lends 
weight to Walter B. Miller’s theory that the genus Sonorella 
Pilsbry, 1900, arose through saltational loss of accessory 
reproductive organs from Eremarionta or an ancestor very 
similar to it (MILLER, 1967; GREGG & MILLER, 1969; 
BEQUAERT & MILLER, 1973). This is because several 
members of the genus Sonorella in the Phoenix area closely 
resemble Eremarionta. These include Sonorella roosevelt- 
zana 8. S. Berry, 1917, and Sonorella allynsmithi Gregg & 
Miller, 1969. These snails resemble the Eremarionta in 
their small size, light shell color, nearly black body wall, 
and their proclivity for the lowest, hottest, and most arid 
habitats (GREGG & MILLER, 1969). 


Acknowledgments 


Thanks are due to the U.S. Fish and Wildlife Service, 
Ecological Services Office in Phoenix, and especially to 
Sally Stefferud for recommending me for the contract for 
the study for which this research was a part. I also thank 
Sally for much patience in helping me with the paperwork 
involved in this research and for taking time out of her 
busy schedule to join me in the field a few times. I would 


Page 432 


also like to thank my mentor and friend Walter B. Miller, 
of the Santa Barbara Museum, who was the person I called 
immediately upon dissecting the first of these snails and 
finding that it was an Eremarionta rather than a Sonorella 
as I had thought. I thank him for much help and guidance 
on this and many other projects. 


Literature Cited 


BEQUAERT, J. C. & W. B. MILLER. 1973. The Mollusks of 
the Arid Southwest with an Arizona Check List. University 
of Arizona Press: Tucson. i-xvi + 1-271 pp. 


Change in Editorship of The Veliger 
Farewell and Thank You from the Departing Editor 


When I was appointed editor of The Veliger in July 
1982, some, even some within the California Malaco- 
zoological Society (CMS), were not certain the journal 
could, or should, continue without its founding editor of 
25 years, R. Stohler. Eleven years and over 4000 journal 
pages later we are still serving our mission—to provide a 
forum for scholarly communication about mollusks. 

That we have been able to continue publishing a quality 
scientific journal is testimony to our readers and to three 
other groups of people I would like to thank: those who 
submitted manuscripts for consideration, those who re- 
viewed the manuscripts, and those who transformed the 
manuscripts and illustrations into a polished, final product. 
Although the editor serves as a facilitator, the quality and 
success of a scientific journal rests largely on the quality 
and abundance of submitted manuscripts, the efforts and 
skills of its reviewers, and the professionalism of the print- 
ing house. Thank you all—readers, authors, reviewers, 
and Allen Press, Inc. 

I feel honored to have been part of the process, and I 
thank CMS for the opportunity to serve the authors and 
readers of The Veliger. I have been especially pleased and 
satisfied by opportunities to assist first-time authors, by 
the growing international and trans-American flavor of 


The Veliger, Vol. 36, No. 4 


GREGG, W. O. & W. B. MILLER. 1969. A new Sonorella from 
Phoenix, Arizona. Nautilus 82(3):90-93. 

MILLER, W.B. 1967. Anatomical revision of the genus Sonorella 
(Pulmonata: Helminthoglyptidae). Doctoral Dissertation, 
University of Arizona, Tucson. 293 pp. 

Pitsspry, H. A. 1939. Land Mollusca of North America (north 
of Mexico). The Academy of Natural Sciences of Philadel- 
phia, Monograph No. 3, Vol. 1, Part 1, i-xi + 1-573 pp. 


the journal (authors in Volume 36 alone represented 18 
countries and 14 states), by the breadth of our reviewer 
base (over 300 different scientists have contributed their 
views on manuscripts), and by the consistently high-qual- 
ity, timely product that the crew at Allen Press, Inc., has 
put out (each of the 42 issues was published exactly on 
the date printed on the cover). 

The future looks bright. May all of you, and your jour- 
nal, fare well indeed. 


D. W. Phillips 


Dr. Barry Roth is New Editor of The Veliger 


CMS has appointed Dr. Barry Roth as Editor of The 
Veliger, and we are cheered that he has accepted the post. 
Dr. Roth, the author of numerous scientific publications 
on land snails and paleontology, is a long-time contributor 
to The Veliger, as an author, a reviewer, and a member of 
the Board of Directors. We are in capable hands. 

Effective immediately, please send all new manuscripts 
to: 


Dr. Barry Roth 

Editor, The Veliger 

745 Cole Street 

San Francisco, CA 94117, USA 


The Veliger 36(4):433-434 (October 1, 1993) 


THE VELIGER 
© CMS, Inc., 1993 


BOOKS, PERIODICALS & PAMPHLETS 


“Larval” and Juvenile Cephalopods: 
A Manual for Their Identification 


edited by M. J. Sweeney, C. F. E. Roper, K. M. 
MANGOLD, M. R. CLARKE & S. Vv. BOLETZKY. Smithsonian 
Contributions to Zoology, no. 513, 282 pp. 


The ecological and economic importance of cephalopods 
in marine ecosystems and fisheries is veiled by our igno- 
rance of the group. Adult squids generally evade capture, 
but young squids, being slower and less maneuverable, are 
more often caught. These stages of the life cycle, however, 
have been the most difficult to identify. By summarizing 
our knowledge of young coleoid cephalopods and providing 
keys, this manual attempts to make their identification 
simpler and directly comparable between workers. Infor- 
mation exchanged among 35 international experts during 
a 1985 workshop forms the basis for this manual. Previ- 
ously published data and figures of young of all described 
coleoid cephalopod families are presented by the 31 con- 
tributors, who, when possible, add new material. Although 
juvenile stages are unknown from some families (e.g., Psy- 
chroteuthidae, Architeuthidae, Neoteuthidae), these fam- 
ilies are included to insure completeness. 

A figured guide to cephalopod terminology (including 
adult characters) begins the volume; a provisional key in- 
tended to enable identification of specimens to the family 
level follows. Although supplemented with an illustrated 
glossary, this key falls short of its objective. The warning 
that family identifications are not to be based solely on the 
key must be heeded. Accurate identifications require ref- 
erence to taxonomic diagnoses and illustrations in the man- 
ual and to additional literature. A table summarizing key 
characters of each family would have been helpful. I sus- 
pect most users will develop their own version of such a 
table, one that includes page references to the pertinent 
sections in the manual. 

The main objective of this volume is accomplished in 
the 26 chapters devoted to the families of Oegopsida (open- 
ocean squids). This volume is the first to provide a nearly 
comprehensive summary of our knowledge of young squids. 
Detailed treatments of these families reveal their morpho- 
logical diversity and often allow identification of genera 
and, sometimes, species. 

The uniform structure of the chapters is a helpful feature 
of the manual, and especially impressive given the diversity 
of authors. Brief diagnoses of adults, young, and eggs are 
followed by a key (or keys) to genus or species level. Both 
adult and juvenile specimens of each genus are figured and 
a short list of recommended references is provided. Ex- 
ceptionally complete and thorough treatments include those 
for the Enoploteuthidae, Ctenopterygidae, Histioteuthi- 


dae, and Cranchiidae. In these families, a wide size range 
of specimens is illustrated in directly comparable figures. 

That the purpose of this volume, to standardize methods 
of identifying young cephalopods, is important can be seen 
by considering the Gonatidae. Much of our knowledge of 
North Pacific gonatid distribution is based on hatchlings 
and juveniles (e.g., KUBODERA & JEFFERTS, 1984a, b). By 
explicitly outlining how species are identified at various 
stages in development, this publication allows other work- 
ers to evaluate these criteria and make comparable deter- 
minations. 

In contrast to the species-level identification possible 
among the young of some open-ocean squids, identification 
of the young from other groups cannot yet be readily ac- 
complished. In a group for which larval identification would 
be most welcome, the myopsid squids of the Loliginidae, 
the potential for larval identification appears to be limited. 
Hatchlings of loliginid species from the well-studied fauna 
of the west North Atlantic can at best be identified to the 
level of genus. In other areas, even generic identifications 
of young are uncertain. 

Among the Octopoda, the low species-level diversity of 
the pelagic and mesopelagic octopods generally allows spe- 
cies-level identification. One quite unexpected inclusion in 
this identification manual is that among the mesopelagic 
octopods of the Bolitaenidae: the genus Dorsopsis is syn- 
onymized with Japetella. 

Among planktonic young of comparatively shallow-wa- 
ter octopodids, chromatophore patterns, rather than mor- 
phological characters, are advocated as the means to iden- 
tify taxa. Although five of the 17 species figured are indicated 
to have been “thoroughly studied,” this section begins with 
the caveat that it cannot be used to identify species; rather 
these 40 pages describe chromatophore organ patterns. 
Given the little morphological variation in octopodids, 
chromatophores may assist in their identification; the ar- 
rangement of chromatophores and suckers, coupled with 
sucker number and arm length patterns, have been shown 
to identify “types” of planktonic octopodids, at least locally 
(YOUNG et al., 1989). If, instead of illustrating a cross- 
section of the octopodid larvae of the world, this chapter 
had addressed octopodids by geographic area, as accom- 
plished in the loliginid treatment, perhaps a measure of 
certainty could have emerged. 

This manual is not free of problems. Most figures have 
been previously published, consistent with the manual’s 
intent to summarize our current knowledge; unfortunately, 
because the figures were produced by diverse illustrators, 
they can be difficult to compare. In some families juveniles 
at the best known or most distinctive stage of the life cycle 
(e.g., the rhyncoteuthion larvae of the Ommastrephidae) 


Page 434 


The Veliger, Vol. 36, No. 4 


are the sole focus of the treatment. More detailed definition 
of critical characters would have been helpful within in- 
dividual chapters. 

To facilitate production of reprints, each family entry 
begins on a recto page. Unfortunately, this makes use of 
the manual awkward; the text often refers to figures on 
the reverse side of the same page. The figures are incon- 
sistently organized on the page. Figure subdivisions are 
located where they fit on the page rather than in a pre- 
dictable pattern. Size indications are generally not included 
on the figures, where they would be discernible at a glance, 
but are included in small print in the captions. 

The seven-year lag between the workshop and publi- 
cation of the volume has created a real liability. Because 
publications later than 1987 are rarely incorporated or 
cited, the volume was out of date prior to its publication. 
Regrettably, YOUNG’s (1991) majer addition to our knowl- 
edge of the chiroteuthids and related groups is not even 
footnoted. As the editors thank the workers who strived 
for timely publication, apparently the delay in publication 
was not due to universal negligence. 

This volume is a comprehensive summary of research 
on planktonic cephalopods, current as of 1987. This de- 
scriptive guide to larval and juvenile cephalopods will 
greatly simplify their identification. Although not all spec- 
imens of all families can be identified with the help of this 


manual, this summary of a scattered literature and explicit 
definition of key characters in identification will prove very 
useful, especially for oegopsid squids. By making this in- 
formation accessible to more scientists and highlighting the 
need for additional work, I hope this volume will attract 
new people to cephalopod biology. An influx of new ideas 
and new approaches to solving old problems is critical if 
this, or any, field of research is to remain vibrant. 


Literature Cited 


KUBODERA, T. & K. JEFFERTS. 1984a. Distribution and abun- 
dance of the early life stages of squid, primarily Gonatidae 
(Cephalopoda, Oegopsida), in the northern North Pacific. 
(Part 1). Bulletin of the National Science Museum, Tokyo 
10A:91-106. 

KUBODERA, T. & K. JEFFERTS. 1984b. Distribution and abun- 
dance of the early life stages of squid, primarily Gonatidae 
(Cephalopoda, Oegopsida), in the northern North Pacific. 
(Part 2). Bulletin of the National Science Museum, Tokyo 
10A:165-193. 

YounG, R. E. 1991. Chiroteuthid and related paralarvae from 
Hawaiian waters. Bulletin of Marine Science 49:162-185. 

YounGc, R. E., R. F. HARMON & F. G. HOCHBERG. 1989. 
Octopodid paralarvae from Hawaiian waters. The Veliger 
32:152-165. 


Janet R. Voigt 


Information for Contributors 


Manuscripts 

Manuscripts must be typed on white paper, 82” by 11”, and double-spaced throughout 
(including references, figure legends, footnotes, and tables). If computer generated copy 
is to be submitted, margins should be ragged right (7.e., not justified). To facilitate the 
review process, manuscripts, including figures, should be submitted in triplicate. The 
first mention in the text of the scientific name of a species should be accompanied by the 
taxonomic authority, including the year, if possible. Underline scientific names and other 
words to be printed in italics. Metric and Celsius units are to be used. 

The sequence of manuscript components should be as follows in most cases: title page, 
abstract, introduction, materials and methods, results, discussion, acknowledgments, lit- 
erature cited, figure legends, figures, footnotes, and tables. The title page should be on a 
separate sheet and should include the title, author’s name, and address. The abstract 
should describe in the briefest possible way (normally less than 200 words) the scope, 
main results, and conclusions of the paper. 


Literature cited 

References in the text should be given by the name of the author(s) followed by the 
date of publication: for one author (Smith, 1951), for two authors (Smith & Jones, 1952), 
and for more than two (Smith et al., 1953). 

The “‘literature cited” section must include all (but not additional) references quoted 
in the text. References should be listed in alphabetical order and typed on sheets separate 
from the text. Each citation must be complete, with all journal titles unabbreviated, and 
in the following form: 


a) Periodicals 
Cate, J. M. 1962. On the identifications of five Pacific Mitra. The Veliger 4:132-134. 


b) Books 


Yonge, C. M. & T. E. Thompson. 1976. Living marine molluscs. Collins: London. 
288 pp. 


c) Composite works 


Feder, H. M. 1980. Asteroidea: the sea stars. Pp. 117-135. In: R. H. Morris, D. P. 
Abbott & E. C. Haderlie (eds.), Intertidal Invertebrates of California. Stanford Univ. 
Press: Stanford, Calif. 


Tables 
Tables must be numbered and each typed on a separate sheet. Each table should be 
headed by a brief legend. 


Figures and plates 

Figures must be carefully prepared and should be submitted ready for publication. 
Each should have a short legend, listed on a sheet following the literature cited. 

Text figures should be in black ink and completely lettered. Keep in mind page format 
and column size when designing figures. 

Photographs for half-tone plates must be of good quality. ‘They should be trimmed off 
squarely, arranged into plates, and mounted on suitable drawing board. Where necessary, 
a scale should be put on the actual figure. Preferably, photographs should be in the 
desired final size. 

It is the author’s responsibility that lettering is legible after final reduction (if any) 
and that lettering size is appropriate to the figure. Charges will be made for necessary 
alterations. 


Processing of manuscripts 

Upon receipt each manuscript is critically evaluated by at least two referees. Based on 
these evaluations the editor decides on acceptance or rejection. Acceptable manuscripts 
are returned to the author for consideration of comments and criticisms, and a finalized 
manuscript is sent to press. The author will receive from the printer two sets of proofs, 
which should be corrected carefully for printing errors. At this stage, stylistic changes 
are no longer appropriate, and changes other than the correction of printing errors will 
be charged to the author at cost. One set of corrected proofs should be returned to the 
editor. 

An order form for the purchase of reprints will accompany proofs. If reprints are 
desired, they are to be ordered directly from the printer. 


Send manuscripts, proofs, and correspondence regarding editorial matters to: Dr. Barry 
Roth, Editor, 745 Cole Street, San Francisco, CA 94117, USA. 


CONTENTS — Continued 


Atlanta californiensis, a new species of atlantid heteropod (Mollusca: Gastropoda) 
from the California Current 
ROGER) RR. SEAPY AND /GOTTHARD: RICHTER ~ ey5 . coy et ne ee 


The gastropod Jerebra santana Loel & Corey, 1932, from the lower Miocene 
Vaqueros Formation, southern California, belongs in the cerithiid genus 
Clavocerithium s.s. 

RICHARD Te SQUIRES ok Ai) Setstag sak RN ani ly Aiea ke ore tod Oe eo 


The validity of Chaetoderma montereyense Heath along with Ch. argenteum Heath 
(Mollusca: Caudofoveata) 
LUITFRIED V. SAL VINISPLAWENG 3). 06 Wve cer ee tee, lee eee 


An empirical evaluation of various techniques for anesthetization and tissue 
fixation of freshwater Unionoida (Mollusca: Bivalvia), with a brief history 
of experimentation in molluscan anesthetization 

CUGLIBTON CONEY) (2c 20628006 2 caine enue yee meee ts i J OI Ae 


NOTES, INFORMATION & NEWS 


Effects of restricted food intake on hemolymph glucose concentration and 
digestive gland—gonad lipid level in the schistosome vector Biomphalaria 
glabrata (Say) (Gastropoda: Planorbidae) 

S:N. THOMPSON AND Ve ,MIEJIA-SCALES) .2)055 .)..:0suy cde heey eee 


Aggressive behavior of the whelk Morula musiva 
INAQ YAGER oo) 21 ot aie cage tiga culgcicgey chap aie Sau ee 


Band color pattern on the venter of a mature shell of Nautilus pompilius 
Linnaeus, 1758 
KENT Di TREC Oi. oie Oh Spee i oc) MN ule) ee Nt hal ee 


Range extension for the land snail Eremarionta rowelli hutsoni (G. H. Clapp, 
1907) 
JAMES DE HIOPEMAN! (7 2). 0). \c eke © aeen ven ee 


Changeun’ editorship of dhe Vel@en. iy) jer ia Aon) an en ee eee 
BOOKS, PERIODICALS: & PAMPBEIE Baisy i ieee 2 aien ete uae ere eae 


om ans Wee 


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